Academia.eduAcademia.edu

Outline

Title
Abstract
Conclusions
References
All Topics
Biology
Evolutionary Biology

Conflict on the sex chromosomes: cause, effect, and complexity

Profile image of Nina WedellNina Wedell

2014, Cold Spring Harbor perspectives in biology

https://doi.org/10.1101/CSHPERSPECT.A017715
visibility

…

description

15 pages

link

1 file

Abstract

Intralocus sexual conflict and intragenomic conflict both affect sex chromosome evolution and can in extreme cases even cause the complete turnover of sex chromosomes. Additionally, established sex chromosomes often become the focus of heightened conflict. This creates a tangled relationship between sex chromosomes and conflict with respect to cause and effect. To further complicate matters, sexual and intragenomic conflict may exacerbate one another and thereby further fuel sex chromosome change. Different magnitudes and foci of conflict offer potential explanations for lineage-specific variation in sex chromosome evolution and answer long-standing questions as to why some sex chromosomes are remarkably stable, whereas others show rapid rates of evolutionary change.

Related papers

On the origin of sex chromosomes
John Lucchesi

BioEssays, 1999

In all living forms, the organization of the genetic material must enable two universally fundamental functions: the elaboration of biological properties and their transmission. In spite of these inexorable commonalties, genomes have a bewildering variety of forms, with differences occurring not only among distant taxa but also, in many instances, between members of the opposite sex within species. The rapidly growing field of comparative genomics offers a powerful tool for unraveling the evolutionary pathways that led to these karyotypic differences. This new method of genetic analysis [Fridolfsson et al,

View PDFchevron_right
Splitting the sexes: The birth and senescence of sex chromosomes
Aivars Cīrulis

Media-Tryck, Lund University, 2022

The evolution of gonochorism from hermaphroditism can be gradual by increasing investment in one sex role while decreasing in the other, or rapid through the fixation of sex-role sterility mutations, eventually leading to the evolution of sex chromosomes. It is expected that the transition will involve a temporary state of gynodioecy or androdioecy as the mutations are not expected to take place at the same time. If the first mutation is a dominant female-sterility mutation, later accompanied by a recessive male sterility mutation, then an XY sex chromosome system evolves, while the opposite combination of mutations will result in a ZW system. Later on sexually antagonistic (SA) genes can be linked to the newly established sex-determining regions on the sex chromosomes. This is followed by recombination arrest in the region, so that the inheritance pattern is sex-limited for all these sex-specific genes. However, the lack of recombination leads to degeneration of the genetic content on the sexlimited chromosomes, since recombination is important for repairing mutations. Nevertheless, recombination arrest does not necessarily mean a dead-end for the sex-limited chromosomes. As our understanding of the very early stages of sex chromosome evolution is mainly based on theory and comparative evidence, we developed a system which we hoped would make it possible to observe in real time what happens after the acquisition of a new sex-determining gene. We used a previously established green fluorescent protein (GFP) line of the simultaneous hermaphrodite Macrostomum lignano. We used the GFP locus as a dominant sterility mutation, which is inherited in a Mendelian fashion. By allowing the GFP allele to be inherited only through sperm, we created male-limited selection lines (resembling the early stages in XY chromosome evolution), and by allowing the GFP allele to be inherited only through egg cells, we created female-limited selection lines (resembling the early stages in ZW chromosome evolution). We also created control lines, where the inheritance pattern was equally mixed. After tens of generations, we investigated how these lines have responded on the level of the genome, the transcriptome, and the phenotype. We sequenced genomes and analysed changes in SNP frequency and structural variant (SV) distribution in pairwise comparisons to see changes across the genome, but particularly on the scaffold where the GFP is located. We also sequenced transcriptomes and performed pairwise comparisons to detect differentially expressed genes, and analysed significant GO terms and KEGG pathways to see how the gene regulation has changed. Besides genomic analyses, we also looked at how mating behaviour (copulation frequency and duration, as well as probability of post-copulatory sucking behaviour) and sexual anatomy (gonad size and morphology of the male copulatory organ called stylet) has changed. We observed that the female-selected lines seemed to have responded the most at the genomic level. For example, the number of significantly differentially expressed transcripts was largest between the female-selected lines and the control lines. These changes seemed to involve downregulation of testes-biased genes. In addition, we observed the highest number of SVs in the female-selected lines, which could be related to changes in recombination rate. In contrast, the male-selected lines seemed to have responded the most at the phenotypic level, since we observed a decrease in the ovary size and body size in the male-selected lines, as well as behavioural changes that may be related to changes in the ejaculate. Both sex-specific selection regimes showed evidence of alterations in the shape of the stylet. Based on these results, we can conclude that our worms have indeed responded to the sex-limited selection in a way that is generally consistent with our expectations from other young sex chromosome systems. The evidence of a decrease in the testes function in the female-selected lines resembles adaptation towards gynodioecy, and the evidence of a decrease in the ovary size in the male-selected lines resembles adaptation towards androdioecy.

View PDFchevron_right
Some Inconvenient Truths About Sex Chromosome Dosage Compensation and the Potential Role of Sexual Conflict
Nina Wedell

Evolution, 2011

Sex chromosome dosage compensation was once thought to be required to balance gene expression levels between sex-linked and autosomal genes in the heterogametic sex. Recent evidence from a range of animals has indicated that although sex chromosome dosage compensation exists in some clades, it is far from a necessary companion to sex chromosome evolution, and is in fact rather rare in animals. This raises questions about why complex dosage compensation mechanisms arise in some clades when they are not strictly needed, and suggests that the role of sex-specific selection in sex chromosome gene regulation should be reassessed. We show there exists a tremendous diversity in the mechanisms that regulate gene dosage and argue that sexual conflict may be an overlooked agent responsible for some of the variation seen in sex chromosome gene dose regulation.

View PDFchevron_right
A Chromosomal Testing Ground Hypothesis for the Evolution of Sexual Reproduction: Sex Chromosomes as Genomic Innovation Centers
Paul D Pruitt

2025

Sexual reproduction remains one of evolution's most perplexing phenomena, given its apparent costs compared to asexual reproduction. Here, we propose a novel hypothesis suggesting that sex chromosomes, particularly the Y chromosome in mammals, serve as genomic "testing grounds" for evolutionary innovations. This hypothesis is based on observed patterns of elevated mutation rates in sex chromosomes and their rapid divergence between closely related species. We suggest that the unique properties of sex chromosomes-including hemizygosity in the heterogametic sex and reduced recombination-create ideal conditions for testing new genetic variants without immediately compromising organismal fitness. This mechanism could provide a previously unrecognized advantage to sexual reproduction by enabling controlled experimentation with genetic innovations.

View PDFchevron_right
The evolution of the peculiarities of mammalian sex chromosomes: an epigenetic view
Eva jablonka

BioEssays, 2004

In most discussions of the evolution of sex chromosomes, it is presumed that the morphological differences between the X and Y were initiated by genetic changes. An alternative possibility is that, in the early stages, a key role was played by epigenetic modifications of chromatin structure that did not depend directly on genetic changes. Such modifications could have resulted from spontaneous epimutations at a sex-determining locus or, in mammals, from selection in females for the epigenetic silencing of imprinted regions of the paternally derived sex chromosome. Other features of mammalian sex chromosomes that are easier to explain if the epigenetic dimension of chromosome evolution is considered include the relatively large number of X-linked genes associated with human brain development, and the overrepresentation of spermatogenesis genes on the X. Both may be evolutionary consequences of dosage compensation through X-inactivation.

View PDFchevron_right
The evolution of restricted recombination in sex chromosomes
Deborah Charlesworth

Trends in Ecology & Evolution, 2009

In species with separate sexes, sex determination often has a genetic basis, and in a wide diversity of taxa a pair of cytologically distinguishable 'sex chromosomes' are found such that the chromosome complements of males and females differ (males are often XY and females XX, but sometimes females are ZW whereas males are ZZ). Recent evidence from sequences of sex-linked genes confirms classical genetic evidence that these chromosomes are a homologous pair, evolved from a normal chromosome pair, between which recombination stopped. We discuss why sex chromosomes evolve reduced recombination and why different parts of the chromosomes stopped recombining at different times, and outline some of the consequences of suppressed recombination, including the evolution of chromosome heteromorphism.

View PDFchevron_right
Genomes of Ellobius species provide insight into the evolutionary dynamics of mammalian sex chromosomes
Wilfred van IJcken

Genome Research, 2016

View PDFchevron_right
Sexually antagonistic coevolution between the sex chromosomes of Drosophila melanogaster
Jessica Abbott

2019

Antagonistic interactions between the sexes are important drivers of evolutionary divergence. Interlocus sexual conflict is generally theorised as a conflict between alleles at two interacting loci whose identity and genomic location are arbitrary. Here we build on previous theory and suggest that when these two loci are located on the X and Y (or Z and W) chromosomes, it can lead to cycles of antagonistic coevolution between the sex chromosomes and the two sexes. To test this hypothesis, we performed experimental crosses using Drosophila melanogaster where we reciprocally exchanged the sex chromosomes between five wild-type populations in a round-robin design. Disrupting putatively coevolved sex chromosome pairs resulted in increased male reproductive success in 16 out of 20 experimental populations (10 of which were significant), but also resulted in lower offspring egg-to-adult viability that affected both male and female fitness. However, after 25 generations of experimental evo...

View PDFchevron_right
Progressive Recombination Suppression and Differentiation in Recently Evolved Neo-sex Chromosomes
Heini Natri

Molecular Biology and Evolution, 2013

Recombination suppression leads to the structural and functional differentiation of sex chromosomes and is thus a crucial step in the process of sex chromosome evolution. Despite extensive theoretical work, the exact processes and mechanisms of recombination suppression and differentiation are not well understood. In threespine sticklebacks (Gasterosteus aculeatus), a different sex chromosome system has recently evolved by a fusion between the Y chromosome and an autosome in the Japan Sea lineage, which diverged from the ancestor of other lineages approximately 2 Ma. We investigated the evolutionary dynamics and differentiation processes of sex chromosomes based on comparative analyses of these divergent lineages using 63 microsatellite loci. Both chromosome-wide differentiation patterns and phylogenetic inferences with X and Y alleles indicated that the ancestral sex chromosomes were extensively differentiated before the divergence of these lineages. In contrast, genetic differentiation appeared to have proceeded only in a small region of the neo-sex chromosomes. The recombination maps constructed for the Japan Sea lineage indicated that recombination has been suppressed or reduced over a large region spanning the ancestral and neo-sex chromosomes. Chromosomal regions exhibiting genetic differentiation and suppressed or reduced recombination were detected continuously and sequentially in the neo-sex chromosomes, suggesting that differentiation has gradually spread from the fusion point following the extension of recombination suppression. Our study illustrates an ongoing process of sex chromosome differentiation, providing empirical support for the theoretical model postulating that recombination suppression and differentiation proceed in a gradual manner in the very early stage of sex chromosome evolution.

View PDFchevron_right
Young sex chromosomes in plants and animals
Deborah Charlesworth

New Phytologist, 2019

Total word count for the main body of the text (Introduction, Materials and Methods, Results, Discussion, and Acknowledgements): 5,944 Word counts for each section 1. Introduction: 1,238 words 2. Properties of initial sex-determining mutations: 2,259 words 3. Has close linkage evolved in response to a sex-determining locus, or did a sexdetermining mutation arise in a pre-existing non-recombining region? 1,432 words 4. Are single-gene systems derived? 840 words 5. The ages of plant and fish sex chromosomes: 280 words 6. Conclusions: 532 words Number of figures (indicating which figures should be published in colour): 3 (all with colours) Number of tables: 0 There is no supporting information

View PDFchevron_right

References (110)

  1. Albert AYK, Otto SP. 2005. Sexual selection can resolve sex- linked sexual antagonism. Science 310: 119-121.
  2. Andolfatto P. 2001. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila mela- nogaster and Drosophila simulans. Mol Biol Evol 18: 279-290.
  3. Arunkumar KP, Mita K, Nagaraju J. 2009. The silkworm Z chromosome is enriched in testis-specific genes. Genetics 182: 493-501.
  4. Bachtrog D. 2013. Y-chromosome evolution: Emerging in- sights into processes of Y-chromosome degeneration. Nat Rev Genet 14: 113-124.
  5. Bachtrog D, Kirkpatrick M, Mank JE, McDaniel SF, Pires JC, Rice WR, Valenzuela N. 2011. Are all sex chromosomes created equal? Trends Genet 27: 350-357.
  6. Bergero R, Forrest A, Kamau E, Charlesworth D. 2007. Evo- lutionary strata on the X chromosomes of the dioecious plant Silene latifolia: Evidence from new sex-linked genes. Genetics 175: 1945-1954.
  7. Blaser O, Grossen C, Neuenschwander S, Perrin N. 2013. Sex-chromosome turnovers induced by deleterious mu- tation load. Evolution 67: 635-645.
  8. Bonduriansky R, Chenoweth SF. 2009. Intralocus sexual conflict. Trends Ecol Evol 24: 280-288.
  9. Burt A, Trivers R. 2006. Genes in conflict: The biology of selfish genetic elements. Harvard University Press, Cambridge MA. Charlesworth D, Charlesworth B. 1980. Sex differences in fitness and selection for centric fusions between sex chro- mosomes and autosomes. Genet Res 35: 205-214.
  10. Charlesworth B, Hartl DL. 1978. Population dynamics of segregation distorter polymorphism of Drosophila mela- nogaster. Genetics 89: 171-192.
  11. Charlesworth D, Mank JE. 2010. The birds and the bees and the flowers and the trees: Lessons from genetic mapping of sex determination in plants and animals. Genetics 186: 9-31.
  12. Charlesworth B, Coyne JA, Barton NA. 1987. The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130: 113-146.
  13. Chase K, Carrier DR, Adler FR, Ostrander EA, Lark KG. 2005. Interaction between the X chromosome and an autosome regulations size sexual dimorphism in Portug- ese water dogs. Genome Res 15: 1820-1824.
  14. Chippindale AK, Rice WR. 2001. Y chromosome polymor- phism is a strong determinant of male fitness in Droso- phila melanogaster. Proc Natl Acad Sci 98: 5677-5682.
  15. Cocquet J, Ellis PJI, Mahadevaiah SK, Affara NA, Vaiman D, Burgoyne PS. 2012. A genetic basis for a postmeiotic X versus Y chromosome intragenomic conflict in the mouse. PLoS Genet 8: e1002900.
  16. Connallon T, Clark AG. 2010. Sex linkage, sex-specific se- lection, and the role of recombination in the evolution of sexually dimorphic gene expression. Evolution 64: 3417- 3442.
  17. Connallon T, Clark AG. 2011a. Association between sex- biased gene expression and mutations with sex-specific phenotypic consequences in Drosophila. Genome Biol Evol 3: 151-155.
  18. Connallon T, Clark AG. 2011b. The resolution of sexual antagonism by gene duplication. Genetics 187: 919-937.
  19. Connallon T, Knowles LL. 2005. Intergenomic conflict re- vealed by patterns of sex-biased gene expression. Trends Genet 21: 495-499.
  20. Cordaux R, Bouchon D, Gre `ve P. 2011. The impact of en- dosymbionts on the evolution of host sex-determination mechanisms. Trends Genet 27: 332 -341.
  21. Dean R, Mank JE. 2014. The role of sex chromosomes in sexual dimorphism: Discordance between molecular and phenotypic data. J Evol Biol doi: 10.1111/jeb.12345.
  22. Dean R, Perry JC, Pizzari T, Mank JE, Wigby S. 2012. Ex- perimental evolution of a novel sexually antagonistic al- lele. PLoS Genet 8: e1002917.
  23. Du ¨bendorfer A, Hediger M, Burghardt G, Bopp D. 2002. Musca domestica: A window on the evolution of sex- determining mechanisms in insects. Int J Dev Biol 46: 75-79.
  24. Ercan S, Giresi PG, Whittle CM, Zhang XM, Green RD, Lieb JD. 2007. X chromosome repression by localization of the C. elegans dosage compensation machinery to sites of transcription initiation. Nat Genet 39: 403-408.
  25. Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Roma- nienko PJ, Camerini-Otero RD, Bonner WM, Manova K, Burgoyne P, Nussenzweig A. 2003. H2AX is required for chromatin remodeling and inactivation of sex chromo- somes in male mouse meiosis. Dev Cell 4: 497-508.
  26. Fisher RA. 1931. The evolution of dominance. Biol Rev 6: 345 -368.
  27. Foerster K, Coulson T, Sheldon BC, Pemberton JM, Clut- ton-Brock TH, Kruuk LEB. 2007. Sexually antagonistic genetic variation for fitness in red deer. Nature 447: 1107-U9.
  28. Frank SA. 1991. Divergence of meiotic drive suppression systems as an explanation for sex-biased hybrid sterility and inviability. Evolution 45: 262 -267.
  29. Gallach M, Betran E. 2011. Intralocus sexual conflict re- solved through gene duplication. Trends Ecol Evol 26: 222 -228.
  30. Gallach M, Chandrasekaran C, Betran E. 2010. Analyses of nuclearly encoded mitochondrial genes suggest gene du- plication as a mechanism for resolving intralocus sexually antagonistic conflict in Drosophila. Genome Biol Evol 2: 835 -850.
  31. Gelbart ME, Kuroda MI. 2009. Drosophila dosage compen- sation: A complex voyage to the X chromosome. Devel- opment 136: 1399-1410.
  32. Gibson JR, Chippindale AK, Rice WR. 2002. The X chro- mosome is a hot spot for sexually antagonistic fitness variation. Proc Biol Sci 269: 499-505.
  33. Good JM. 2012. The conflict within and the escalating war between the sex chromosomes. PLoS Genet 8: e1002955.
  34. Griffin RM, Dean R, Grace JL, Ryden P, Friberg U. 2013. The shared genome is a pervasive constraint on the evolution of sex-biased gene expression. Mol Biol Evol 30: 2168- 2176.
  35. Guioli S, Lovell-Badge R, Turner JMA. 2012. Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line. PLoS Genet 8: e1002560.
  36. Hahn MW, Lanzaro GC. 2005. Female-biased gene expres- sion in the malaria mosquito Anopheles gambiae. Curr Biol 15: R192-R193.
  37. Hall DW. 2004. Meiotic drive and sex chromosome cycling. Evolution 58: 925-931.
  38. Hamilton WD. 1967. Extraordinary sex ratios. Science 156: 477-488.
  39. Harrison P, Mank JE, Wedell. 2012. Incomplete sex chromo- some dosage compensation in the Indian meal moth, Plodia interpunctella, based on de novo transcriptome assembly. Genome Biol Evol 4: 1118-1126.
  40. Hense W, Baines JF, Parsch J. 2007. X chromosome inacti- vation during Drosophila spermatogenesis. PLoS Biol 5: 2288-2295.
  41. Hosken DJ, Stockley P, Tregenza T, Wedell N. 2009. Monog- amy and the battle of the sexes. Annu Rev Entomol 54: 361-378.
  42. Hughes JF, Skaletsky H, Brown LG, Pyntikova T, Graves T, Fulton RS, Dugan S, Ding Y, Buhay CJ, Kremitzki C, et al. 2012. Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes. Nature 483: 82-124.
  43. Hurst LD, Pomiankowski A. 1991. Causes of sex-ratio bias may account for unisexual sterility in hybrids. A new explanation of Haldane's Rule and related phenomena. Genetics 128: 841-845.
  44. A, Schielzeth H, Forstmeier W, Gustafsson L, Qvarn- strom A. 2013. Sex chromosome linked genetic variance and the evolution of sexual dimorphism of quantitative traits. Evolution 67: 609-619.
  45. Innocenti P, Morrow EH. 2010. The sexually antagonistic genes of Drosophila melanogaster. PLoS Biol 8: e1000335.
  46. Itoh Y, Melamed E, Yang X, Ka PK, Wang S, Yehya N, van Nas A, Replogle K, Band MR, Clayton DF, et al. 2007. Dosage compensation is less effective in birds than in mammals. J Biol 6: 2.
  47. Iyengar VK, Reeve HK, Eisner T. 2002. Paternal inheritance of a female moth's mating preference. Nature 419: 830 - 832.
  48. Jaenike J. 2001. Sex chromosome meiotic drive. Annu Rev Ecol Syst 32: 25-49.
  49. Jaquiery J, Rispe C, Roze D, Legeai F, Le Trionnaire G, Stoeckel S, Mieuzet L, Da Silva C, Poulain J, Prunier- Leterme N, et al. 2013. Masculinization of the X chro- mosome in the pea aphid. PLoS Genet 9: e1003690.
  50. Julien P, Brawand D, Soumillon M, Necsulea A, Liechti A, Schutz F, Daish T, Grutzner F, Kaessmann H. 2012. Mech- anisms and evolutionary patterns of mammalian and avian dosage compensation. PLoS Biol 10: e100128.
  51. Kaiser B, Bachtrog D. 2010. Evolution of sex chromosomes in insects. Annu Rev Genet 44: 91-112.
  52. Khil PP, Smirnova NA, Romanienko PJ, Camerini-Otero RD. 2004. The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat Genet 36: 642-646.
  53. Kitano J, Ross JA, Mori S, Kume M, Jones FC, Chan YF, Absher DM, Grimwood J, Schmutz J, Myers RM, et al. 2009. A role for a neo-sex chromosome in stickleback speciation. Nature 461: 1079-1083.
  54. Koerich LB, Wang XY, Clark AG, Carvalho AB. 2008. Low conservation of gene content in the Drosophila Y chro- mosome. Nature 456: 949 -951.
  55. Kondo M, Nanda I, Hornung U, Asakawa S, Shimizu N, Mitani H, Schmid M, Shima A, Schartl M. 2003. Ab- sence of the candidate male sex-determining gene dmrt1b(Y) of medaka from other fish species. Curr Biol 13: 416 -420.
  56. Lahn BT, Page DC. 1999. Four evolutionary strata on the human X chromosome. Science 286: 964-967.
  57. Lange J, Skaletsky H, van Daalen SKM, Embry SL, Korver CM, Brown LG, Oates RD, Silber S, Repping S, Page DC. 2009. Isodicentric Y chromosomes and sex disorders as byproducts of homologous recombination that main- tains palindromes. Cell 138: 855-869.
  58. Lemos B, Branco AT, Hartl DL. 2010. Epigenetic effects of polymorphic Y chromosomes modulate chromatin com- ponents, immune response, and sexual conflict. Proc Natl Acad Sci 107: 15826-15831.
  59. Livernois AM, Waters SA, Deakin JE, Graves JAM, Waters PD. 2013. Independent evolution of transcriptional inac- tivation on sex chromosomes in birds and mammals. PLoS Genet 9: e1003635.
  60. Mank JE. 2009. The W, X, Y and Z of sex chromosome dosage compensation. Trends Genet 25: 226 -233.
  61. Mank JE. 2013. Sex chromosome dosage compensation, definitely not for everyone. Trends Genet 29: 677 -683.
  62. Mank JE, Ellegren H. 2007. Parallel divergence and degra- dation of the avian W sex chromosome. Trends Ecol Evol 22: 389-391.
  63. Mank JE, Hosken DJ, Wedell N. 2011. Some inconvenient trusts about sex chromosome dosage compensation and the potential role of sexual conflict. Evolution 65: 2133- 2144.
  64. Marais GAB, Campos PRA, Gordo I. 2010. Can intra-Y conversion oppose the degeneration of the human Y chromosome: A simulation study. Genome Biol Evol 2: 347 -357
  65. Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, et al. 2002. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Na- ture 417: 559 -563.
  66. Meiklejohn CD, Tao Y. 2010. Genetic conflict and sex chro- mosome evolution. Trends Ecol Evol 25: 215 -223.
  67. Meiklejohn CD, Landeen EL, Cook JM, Kingan SB, Pre- sgraves DC. 2011. Sex chromosome-specific regulation in the Drosophila male germline but little evidence for chromosomal dosage compensation or meiotic inactiva- tion. PLoS Biol 9: e1001126.
  68. Meisel RP, Han MV, Hahn MW. 2009. A complex suite of forces drives gene traffic from Drosophila X chromo- somes. Genome Biol Evol 1: 176 -188.
  69. Meisel RP, Malone JH, Clark AG. 2012. Disentangling the relationship between sex-biased gene expression and X- linkage. Genome Res 22: 1255-1265.
  70. Miura I. 2007. An evolutionary witness: The frog Rana ru- gosa underwent change of heterogametic sex from XY male to ZW female. Sex Dev 1: 323-331.
  71. Moghadam HK, Pointer MA, Wright AE, Berlin S, Mank JE. 2012. W chromosome expression responds to female- specific selection. Proc Natl Acad Sci 109: 8207-8211.
  72. Mueller JL, Mahadevaiah SK, Park PJ, Warburton PE, Page DC, Turner JMA. 2008. The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. Nat Genet 40: 794-799.
  73. Muyle A, Zemp N, Deschamps C, Mousset S, Widmer A, Marais GAB. 2012. Rapid de novo evolution of X chro- mosome dosage compensation in Silene latifolia, a plant with young sex chromosomes. PLoS Biol 10: e1001308.
  74. Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan ZH, Haaf T, Shimizu N, Shima A, et al. 2002. A duplicated copy of DMRT1 in the sex-deter- mining region of the Y chromosome of the medaka, Or- yzias latipes. Proc Natl Acad Sci 99: 11778-11783.
  75. Natri HM, Shikano T, Merila J. 2013. Progressive recombi- nation suppression and differentiation in recently evolved neo-sex chromosomes. Mol Biol Evol 30: 1131-1144.
  76. Nolte V, Pandey RM, Kofler R, Schlotterer C. 2013. Genome- wide patterns of natural variation reveal string selective sweeps and ongoing genomic conflict in Drosophila mauritiana. Genome Res 23: 99-110.
  77. Ogata M, Hasegawa Y, Ohtani H, Mineyama M, Miura I. 2008. The ZZ/ZW sex-determining mechanism originat- ed twice and independently during evolution of the frog, Rana rugosa. Heredity 100: 92-99.
  78. Partridge L, Hurst LD. 1998. Sex and conflict. Science 281: 2003-2008.
  79. Pointer MA, Harrison PW, Wright AE, Mank JE. 2013. Mas- culinization of gene expression is associated with exag- geration of male sexual dimorphism. PLoS Genet 9: e1003697.
  80. Poissant J, Wilson AJ, Coltman DW. 2010. Sex-specific ge- netic variance and the evolution of sexual dimorphism: A systematic review of cross-sex genetic correlations. Evo- lution 64: 97-107.
  81. Postma E, Spyrou N, Rollins LA, Brooks RC. 2011. Sex- dependent selection differentially shapes genetic varia- tion on and off the guppy Y chromosome. Evolution 65: 2145-2156.
  82. Potrzebowski L, Vinckenbosch N, Marques AC, Chalmel F, Jegou B, Kaessmann H. 2008. Chromosomal gene move- ments reflect the recent origin and biology of therian sex chromosomes. PLoS Biol 6: 709-716.
  83. Presgraves, DC. 2010. The molecular evolutionary basis of species formation. Nat Rev Genet 11: 175 -180.
  84. Price TAR, Wedell N. 2004. Selfish genetic elements and sexual selection: Their impact on male fertility. Genetica 132: 295-307.
  85. Rice WR. 1984. Sex chromosomes and the evolution of sex- ual dimorphism. Evolution 38: 735 -742.
  86. Rice WR. 1987. The accumulation of sexually antagonistic genes as a selection agent promoting the evolution of reduced recombination between primitive sex chromo- somes. Evolution 41: 911-914.
  87. Roberts RB, Ser JR, Kocher TD. 2009. Sexual conflict re- solved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 326: 998-1001.
  88. Sackton TB, Montenegro H, Hartl DL, Lemos B. 2011. In- terspecific Y chromosome introgressions disrupt testis- specific gene expression and male reproductive pheno- types in Drosophila. Proc Natl Acad Sci 108: 17046- 17051.
  89. Saether SA, Saetre GP, Borge T, Wiley C, Svedin N, Ander- sson G, Veen T, Haavie J, Servedio MR, Bures S, et al. 2007. Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318: 95-97.
  90. Saetre GP, Borge T, Lindroos K, Haavie J, Sheldon BC, Prim- mer C, Syvanen AC. 2003. Sex chromosome evolution and speciation in Ficedula flycatchers. Proc Biol Sci 270: 53-59.
  91. Sayres MAW, Makova KD. 2011. Genome analyses substan- tiate male mutation bias in many species. Bioessays 33: 938 -945.
  92. Schoenmakers S, Wassenaar E, Hoogerbrugge JW, Laven JSE, Grootegoed JA, Baarends WM. 2009. Female meiotic sex chromosome inactivation in chicken. PLoS Genet 5: e100466.
  93. Straub T, Becker PB. 2007. Dosage compensation: The beginning and end of generalization. Nat Rev Genet 8: 47-57.
  94. Toups MA, Pease JB, Hahn MW. 2011. No excess gene move- ment is detected off the avian or lepidopteran Z chromo- some. Genome Biol Evol 3: 1463-1472.
  95. van Doorn GS, Kirkpatrick M. 2007. Turnover of sex chro- mosomes induced by sexual conflict. Nature 449: 909- 912.
  96. van Doorn GS, Kirkpatrick M. 2010. Transitions between male and female heterogamety caused by sex-antagonis- tic selection. Genetics 186: 629-U294.
  97. Vibranovski MD, Zhang Y, Long MY. 2009. General gene movement off the X chromosome in the Drosophila ge- nus. Genome Res 19: 897-903.
  98. Vicoso B, Bachtrog D. 2011. Lack of global dosage compen- sation in Schistosoma mansoni, a female-heterogametic parasite. Genome Biol Evol 3: 230-235.
  99. Vicoso B, Bachtrog D. 2013. Reversal of an ancient sex chromosome to an autosome in Drosophila. Nature 499: 332.
  100. Vicoso B, Charlesworth B. 2009. The deficit of male-biased genes on the D. melanogaster X chromosome is expres- sion-dependent: A consequence of dosage compensa- tion? J Mol Evol 68: 576-583.
  101. Vicoso B, Charlesworth B. 2010. Effective population size and the faster-X effect: An extended model. Evolution 63: 2413-2426.
  102. Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D. 2013. Comparative sex chromosome genomics in snakes: Differentiation, evolutionary strata and lack of global dosage compensation. PLoS Biol 11: e1001643.
  103. Wedell N. 2013. The dynamic relationship between polyan- dry and selfish genetic elements. Phil Trans R Soc 368: 1 -10.
  104. Werren JH, Beukeboom LW. 1998. Sex determination, sex ratios, and genetic conflict. Annu Rev Ecol Syst 29: 233- 261.
  105. Wilkinson GS, Johns PM, Metheny JD, Baker RH. 2013. Sex-biased gene expression during head development in a sexually dimorphic stalk-eyed fly. PLoS ONE 8: e59826.
  106. Winge O ¨. 1927. The location of eighteen genes in Lebistes reticulata. J Genet 18: 1-43.
  107. Wolfenbarger LL, Wilkinson GS. 2001. Sex-linked expres- sion of a sexually selected trait in the stalk-eyed fly, Cy- rtodiopsis dalmanni. Evolution 55: 103-110.
  108. Wright AE, Moghadam HK, Mank JE. 2012. Trade-off be- tween selection for dosage compensation and masculin- ization on the avian Z chromosome. Genetics 192: 1433- 1445.
  109. Yoshida K, Kitano J. 2012. The contribution of female mei- otic drive to the evolution of neo-sex chromosomes. Evo- lution 66: 3198-3208.
  110. Zhou Q, Bachtrog D. 2012. Chromosome-wide gene silencing initiate Y-degeneration in Drososphila. Curr Biol 22: 522-525. October 3, 2014 2014; doi: 10.1101/cshperspect.a017715 originally published online Cold Spring Harb Perspect Biol Judith E. Mank, David J. Hosken and Nina Wedell

Related papers

Genetic conflict and sex chromosome evolution
Colin Meiklejohn

Trends in Ecology & Evolution, 2010

Chromosomal sex determination systems create the opportunity for the evolution of selfish genetic elements that increase the transmission of one sex chromosome at the expense of its homolog. Because such selfish elements on sex chromosomes can reduce fertility and distort the sex ratio of progeny, unlinked suppressors are expected to evolve, bringing different regions of the genome into conflict over the meiotic transmission of the sex chromosomes. Here we argue that recurrent genetic conflict over sex chromosome transmission is an important evolutionary force that has shaped a wide range of seemingly disparate phenomena including the epigenetic regulation of genes expressed in the germline, the distribution of genes in the genome, and the evolution of hybrid sterility between species.

View PDFchevron_right
Sex chromosome evolution: historical insights and future perspectives
Jessica Abbott

Proceedings of the Royal Society B: Biological Sciences, 2017

Many separate-sexed organisms have sex chromosomes controlling sex determination. Sex chromosomes often have reduced recombination, specialized (frequently sex-specific) gene content, dosage compensation and heteromorphic size. Research on sex determination and sex chromosome evolution has increased over the past decade and is today a very active field. However, some areas within the field have not received as much attention as others. We therefore believe that a historic overview of key findings and empirical discoveries will put current thinking into context and help us better understand where to go next. Here, we present a timeline of important conceptual and analytical models, as well as empirical studies that have advanced the field and changed our understanding of the evolution of sex chromosomes. Finally, we highlight gaps in our knowledge so far and propose some specific areas within the field that we recommend a greater focus on in the future, including the role of ecology ...

View PDFchevron_right
Steps in the evolution of heteromorphic sex chromosomes
Deborah Charlesworth

Heredity, 2005

We review some recently published results on sex chromosomes in a diversity of species. We focus on several fish and some plants whose sex chromosomes appear to be 'young', as only parts of the chromosome are nonrecombining, while the rest is pseudoautosomal. However, the age of these systems is not yet very clear. Even without knowing what proportions of their genes are genetically degenerate, these cases are of great interest, as they may offer opportunities to study in detail how sex chromosomes evolve. In particular, we review evidence that recombination suppression occurs progressively in evolutionarily independent cases, suggesting that selection drives loss of recombination over increasingly large regions. We discuss how selection during the period when a chromosome is adapting to its role as a Y chromosome might drive such a process.

View PDFchevron_right
The evolution of heteromorphic sex chromosomes
John Lucchesi

BioEssays, 1994

View PDFchevron_right
The genetics of sex chromosomes: evolution and implications for hybrid incompatibility
Norman Johnson

Annals of the New York Academy of Sciences, 2012

Heteromorphic sex chromosomes, where one sex has two different types of sex chromosomes, face very different evolutionary consequences than do the autosomes. Two important features of sex chromosomes arise from being present in only copy in one of the sexes: dosage compensation and the meiotic silencing of sex chromosomes. Other differences arise because sex chromosomes spend unequal amounts of time in each sex. Thus, the impact of evolutionary processes (mutation, selection, genetic drift, and meiotic drive) differs substantially between each sex chromosome, and between the sex chromosomes and the autosomes. Sex chromosomes also play a disproportionate role in Haldane's rule and other important patterns related to hybrid incompatibility, and thus speciation. We review the consequences of sex chromosomes on hybrid incompatibility. A theme running through this review is that epigenetic processes, notably those related to chromatin, may be more important to the evolution of sex chromosomes and the evolution of hybrid incompatibility than previously recognized.

View PDFchevron_right

Related topics

  • Evolutionary Biology
  • Genetics
  • Evolution of Sexual Reproduction
  • Sexual Conflict
  • Biology
  • Medicine
  • Sex chromosomes
  • Sex Factors

    • Cited by

    Eukaryote hybrid genomes
    Joana Meier

    PLOS Genetics

    Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adaptation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve.

    View PDFchevron_right
    The Diversity and Evolution of Sex Chromosomes in Frogs
    Wen-Juan Ma

    Genes

    Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromoso...

    View PDFchevron_right
    ZZ Top: faster and more adaptive Z chromosome evolution in two Lepidoptera
    Megan Hansen

    The rate of divergence for Z or X chromosomes is theoretically predicted to be greater than autosomes, but the possible explanations for this pattern vary, as do empirical results from diverse taxa. Even among moths and butterflies (Lepidoptera), which generally share a single-origin Z chromosome, the handful of available studies give mixed support for faster or more adaptive evolution of the Z chromosome, depending on the species assayed. Here, we examine the molecular evolution of Z chromosomes in two additional lepidopteran species: the Carolina sphinx moth and the monarch butterfly, the latter of which possesses a recent chromosomal fusion yielding a segment of newly Z-linked DNA. We find evidence for both faster and more adaptive Z chromosome evolution in both species, though this effect is strongest in the neo-Z portion of the monarch sex chromosome. The neo-Z is less male-biased than expected of a Z chromosome, and unbiased and female-biased genes drive the signal for adaptiv...

    View PDFchevron_right
    Diversity of Modes of Reproduction and Sex Determination Systems in Invertebrates, and the Putative Contribution of Genetic Conflict
    Hector Escriva

    Genes, 2021

    About eight million animal species are estimated to live on Earth, and all except those belonging to one subphylum are invertebrates. Invertebrates are incredibly diverse in their morphologies, life histories, and in the range of the ecological niches that they occupy. A great variety of modes of reproduction and sex determination systems is also observed among them, and their mosaic-distribution across the phylogeny shows that transitions between them occur frequently and rapidly. Genetic conflict in its various forms is a long-standing theory to explain what drives those evolutionary transitions. Here, we review (1) the different modes of reproduction among invertebrate species, highlighting sexual reproduction as the probable ancestral state; (2) the paradoxical diversity of sex determination systems; (3) the different types of genetic conflicts that could drive the evolution of such different systems.

    View PDFchevron_right
    Recessive Z-linked lethals and the retention of haplotype diversity in a captive butterfly population
    Carl yung

    Heredity, 2020

    Sex chromosomes are predicted to harbour elevated levels of sexually antagonistic variation due to asymmetries in the heritability of recessive traits in the homogametic versus heterogametic sex. This evolutionary dynamic may manifest as high recessive load specifically affecting the homogametic sex, and the retention of haplotype diversity in small populations. We tested the hypothesis that the Z chromosome in the butterfly Bicyclus anynana carries a high inbred load for male fertility and viability. Homozygosity of Z chromosome blocks was produced by daughter-father backcrosses, and inferred from marker loci positioned via a linkage map. Male sterility was, in general, unrelated to homozygosity in any region of the Z, but there was an extreme deficit of homozygous males within a 2 cM interval in all families. In contrast, no corresponding skew in Z genotype was detected in their (hemizygous) sisters. The same pattern was observed in historically inbred lines, indicating a high frequency of recessive lethals in the ancestral population. Allele-frequency changes between 1993 and 2006 (70 generations at N e~1 60) show that, despite the loss of many haplotypes, diversity was retained significantly above the neutral expectation. Effective overdominance in the lethal region can account for this effect locally but not in other parts of the chromosome, that are also associated with persistent linkage disequilibrium. These unexpected patterns suggest the operation of other factors, such as epistatic selection, recombination suppression, assortative mating and meiotic drive. Our results highlight the role of balancing selection in maintaining the inbred load and linked genetic diversity.

    View PDFchevron_right
    580 California St., Suite 400
    San Francisco, CA, 94104
    © 2025 Academia. All rights reserved