CoChat
Sign Up
Cited by 178Genetic and Clinical Aspects of Sex Determination and Chromosomal AbnormalitiesChromosomal and Genetic VariationsReproductive biology and impacts on aquatic species

Turnover of sex chromosomes and speciation in fishes

Open access
Kitano, Jun, Peichel, Catherine L.·2012·Environmental Biology of Fishes
DOI 10.1007/s10641-011-9853-8PMC PMC4459657
Open this paper in CoChat — free accountOpen PDF

Abstract

Closely related species of fishes often have different sex chromosome systems. Such rapid turnover of sex chromosomes can occur by several mechanisms, including fusions between an existing sex chromosome and an autosome. These fusions can result in a multiple sex chromosome system, where a species has both an ancestral and a neo-sex chromosome. Although this type of multiple sex chromosome system has been found in many fishes, little is known about the mechanisms that select for the formation of neo-sex chromosomes, or the role of neo-sex chromosomes in phenotypic evolution and speciation. The identification of closely related, sympatric species pairs in which one species has a multiple sex chromosome system and the other has a simple sex chromosome system provides an opportunity to study sex chromosome turnover. Recently, we found that a population of threespine stickleback (Gasterosteus aculeatus) from Japan has an X1X2Y multiple sex chromosome system resulting from a fusion between the ancestral Y chromosome and an autosome, while a sympatric threespine stickleback population has a simple XY sex chromosome system. Furthermore, we demonstrated that the neo-X chromosome (X 2) plays an important role in phenotypic divergence and reproductive isolation between these sympatric stickleback species pairs. Here, we review multiple sex chromosome systems in fishes, as well as recent advances in our understanding of the evolutionary role of sex chromosome turnover in stickleback speciation.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1007/s10641-011-9853-8

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Robertsonian fusions can result in the recruitment of autosomes into becoming sex chromosomes, as has been seen in fishes.

    “On the scale of whole chromosomes, dramatic changes like Robertsonian fusions can result in the recruitment of autosomes into becoming sex chromosomes, as has been seen in fishes (155)”

    From Topological Approaches in Animal Comparative Genomics (2026) · cites this paper as [155]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 64

  1. Almeida-Toledo LF Daniel-Silva MFZ Lopes CE Toledo-Filho SA Sex chromosome evolution in fish. II. Second occurrence of an X1X2Y sex chromosome system in Gymnotiformes Chrom Res 2000 8 335 340 10.1023/A:1009287630301 10919724 · DOI
  2. Almeida-Toledo LF Foresti F Daniel MFZ Toledo SA Sex chromosome evolution in fish: the formation of the neo-Y chromosome in Eigenmannia (Gymnotiformes) Chromosoma 2000 109 3 197 200 10.1007/s004120050428 10929198 · DOI
  3. Almeida-Toledo LF Foresti H Toledo-Filho SA Complex sex chromosome system in Eigenmannia sp. (Pisces, Gymnotiformes) Genetica 1984 64 165 169 10.1007/BF00115340 · DOI
  4. Alves AL Oliveira C Nirchio M Granado A Foresti F Karyotypic relationships among the tribes of Hypostominae (Siluriformes: Loricariidae) with description of XO sex chromosome system in a Neotropical fish species Genetica 2006 128 1 9 10.1007/s10709-005-0715-1 17028935 · DOI
  5. Bachtrog D Accumulation of spock and worf, two novel non-LTR retrotransposons, on the neo-Y chromosome of Drosophila miranda Mol Biol Evol 2003 20 173 181 10.1093/molbev/msg035 12598683 · DOI
  6. Bachtrog D Evidence that positive selection drives Y-chromosome degeneration in Drosophila miranda Nat Genet 2004 36 518 522 10.1038/ng1347 15107853 · DOI
  7. Bachtrog D Expression profile of a degenerating neo-Y chromosome in Drosophila Curr Biol 2006 16 1694 1699 10.1016/j.cub.2006.07.053 16950105 · DOI
  8. Bachtrog D Charlesworth B Reduced adaptation of a non-recombining neo-Y chromosome Nature 2002 416 323 326 10.1038/416323a 11907578 · DOI
  9. Bachtrog D Hom E Wong KM Maside X de Jong P Genomic degradation of a young Y chromosome in Drosophila miranda Genome Biol 2008 9 R30 10.1186/gb-2008-9-2-r30 18269752 PMC2374705 · DOI
  10. Bachtrog D Jensen JD Zhang Z Accelerated adaptive evolution on a newly formed X chromosome PLoS Biol 2009 7 e1000082 10.1371/journal.pbio.1000082 PMC2672600 19402745 · DOI
  11. Bertollo LAC Born GG Dergam JA Fenocchio AS Moreira-Filho O A biodiversity approach in the neotropical Erythrinidae fish, Hoplias malabaricus. Karyotypic survey, geographic distribution of cytotypes and cytotaxonomic considerations Chrom Res 2000 8 603 613 10.1023/A:1009233907558 11117356 · DOI
  12. Bertollo LAC Chromosome evolution in the erythrinid fish, Erythrinus erythrinus (Teleostei: Characiformes) Heredity 2004 93 228 233 10.1038/sj.hdy.6800511 15241446 · DOI
  13. Bertollo LAC Takahashi CS Moreira-Filho O Multiple sex chromosomes in the genus Hoplias (Pisces: Erythrinidae) Cytologia 1983 48 1 1 12 10.1508/cytologia.48.1 · DOI
  14. Caputo V Machella N Nisi-Cerioni P Olmo E Cytogenetics of nine species of Mediterranean blennies and additional evidence for an unusual multiple sex-chromosome system in Parablennius tentacularis (Perciformes, Blenniidae) Chrom Res 2001 9 3 12 10.1023/A:1026779314932 11272790 · DOI
  15. Centofante L Bertollo LA Moreira-Filho O Cytogenetic characterization and description of an XX/XY1Y2 sex chromosome system in catfish Harttia carvalhoi (Siluriformes, Loricariidae) Cytogenet Genome Res 2006 112 3–4 320 324 10.1159/000089887 16484789 · DOI
  16. Charlesworth D Charlesworth B Sex differences in fitness and selection for centric fusions between sex-chromosomes and autosomes Genet Res 1980 35 205 214 10.1017/S0016672300014051 6930353 · DOI
  17. Cioffi MB Bertollo LA Initial steps in XY chromosome differentiation in Hoplias malabaricus and the origin of an X1X2Y sex chromosome system in this fish group Heredity 2010 105 554 561 10.1038/hdy.2010.18 20216570 · DOI
  18. Devlin RH Nagahama Y Sex determination and sex differentiation in fish: overview of genetic, physiological, and environmental influences Aquaculture 2002 208 191 364 10.1016/S0044-8486(02)00057-1 · DOI
  19. Ewulonu UK Haas R Turner BJ A multiple sex chromosome system in the annual killifish, Nothobranchius guentheri Copeia 1985 1985 503 508 10.2307/1444868 · DOI
  20. Henning F Trifonov V Ferguson-Smith MA de Almeida-Toledo LF Non-homologous sex chromosomes in two species of the genus Eigenmannia (Teleostei: Gymnotiformes) Cytogenetic Genome Res 2008 121 1 55 58 10.1159/000124382 18544927 · DOI
  21. Higuchi M Goto A Genetic evidence supporting the existence of two distinct species in the genus Gasterosteus around Japan Environ Biol Fish 1996 47 1 16 10.1007/BF00002375 · DOI
  22. Jesus CM Bertollo LAC Moreira-Filho O Comparative cytogenetics in Apareiodon affinis (Pisces, Characiformes) and considerations regarding diversification of the group Genetica 1999 105 63 67 10.1023/A:1003592022927 · DOI
  23. Kingsley DM Peichel CL Ostlund-Nilsson S Mayer I Huntingford FA The molecular genetics of evolutionary change in sticklebacks Biology of the Three-spined Stickleback 2007 Boca Raton CRC Press 41 81
  24. Kitano J Mori S Peichel CL Phenotypic divergence and reproductive isolation between sympatric forms of Japanese threespine sticklebacks Biol J Linn Soc 2007 91 671 685 10.1111/j.1095-8312.2007.00824.x · DOI
  25. Kitano J Mori S Peichel CL Sexual dimorphism in the external morphology of the threespine stickleback (Gasterosteus aculeatus) Copeia 2007 2007 336 349 10.1643/0045-8511(2007)7[336:SDITEM]2.0.CO;2 · DOI
  26. Kitano J A role for a neo-sex chromosome in stickleback speciation Nature 2009 461 7267 1079 1083 10.1038/nature08441 19783981 PMC2776091 · DOI
  27. Kondo M Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka Genome Res 2006 16 815 826 10.1101/gr.5016106 16751340 PMC1484449 · DOI
  28. Kume M Kitamura T Takahashi H Goto A Distinct spawning migration patterns in sympatric Japan Sea and Pacific Ocean forms of threespine stickleback Gasterosteus aculeatus Ichthyol Res 2005 52 189 193 10.1007/s10228-005-0269-3 · DOI
  29. Kume M Kitano J Mori S Shibuya T Ecological divergence and habitat isolation between two migratory forms of Japanese threespine stickleback (Gasterosteus aculeatus) J Evol Biol 2010 23 1436 1446 10.1111/j.1420-9101.2010.02009.x 20456572 · DOI
  30. Lindholm A Breden F Sex chromosomes and sexual selection in Poeciliid fishes Am Nat 2002 160 S214 S224 10.1086/342898 18707478 · DOI
  31. Mank JE Promislow DEL Avise JC Evolution of alternative sex-determining mechanisms in teleost fishes Biol J Linn Soc 2006 87 83 93 10.1111/j.1095-8312.2006.00558.x · DOI
  32. Margarido VP Bellafronte E Moreira-Filho O Cytogenetic analysis of three sympatric Gymnotus (Gymnotiformes, Gymnotidae) species verifies invasive species in the Upper Parana River basin, Brazil J Fish Biol 2007 70 155 164 10.1111/j.1095-8649.2007.01365.x · DOI
  33. Morescalchi A Hureau JC Olmo E Ozouf-Costaz C Pisano E Stanyon R A multiple sex-chromosome system in Antarctic ice-fishes Polar Biol 1992 11 655 661 10.1007/BF00237962 · DOI
  34. Moyle LC Muir CD Han MV Hahn MW The contribution of gene movement to the “two rules of speciation” Evolution 2010 64 1541 1557 10.1111/j.1558-5646.2010.00990.x 20298429 · DOI
  35. Murofushi M Nishikawa S Yosida TH Cytogenetical studies on fishes. V. Multiple sex chromosome mechanism (XX-Y) found in two dragonet fishes Proc Jpn Acad B Phys Biol Sci 1983 59 58 61 10.2183/pjab.59.58 · DOI
  36. Murofushi M Oikawa S Nishikawa S Yosida TH Cytogenetical studies on fishes. III. Multiple sex chromosome mechanism in the filefish, Stephanolepis cirrhifer Jpn J Genet 1980 55 2 127 132 10.1266/jjg.55.127 · DOI
  37. Murofushi M Yosida TH Cytogenetical studies on fishes. VIII. XX-Y sex chromosome mechanism newly found in the snake eel, Muraenichthys gymnotus (Anguilloform, Pisces) Proc Jpn Acad Ser B Phys Biol Sci 1984 60 2 21 23 10.2183/pjab.60.21 · DOI
  38. Ojima Y Kikuno T A heteromorphic chromosome of Beryx splendens, Berycidae (Pisces) Proc Jpn Acad B Phys Biol Sci 1986 62 317 320 10.2183/pjab.62.317 · DOI
  39. Oliveira C Almeida-Toledo LF Evidence of an XX/XY sex chromosome system in the fish Dormitator maculatus (Teleostei, Eleotrididae) Genet Mol Biol 2006 29 653 655 10.1590/S1415-47572006000400013 · DOI
  40. Oliveira RR Feldberg E dos Anjos MB Zuanon J Occurrence of multiple sexual chromosomes (XX/XY1Y2 and Z1Z1Z2Z2/Z1Z2W1W2) in catfishes of the genus Ancistrus (Siluriformes, Loricariidae) from the Amazon Basin Genetica 2008 134 2 243 249 10.1007/s10709-007-9231-9 18038220 · DOI
  41. Pezold F Evidence for multiple sex chromosomes in the freshwater goby, Gobionellus shufeldti (Pisces: Gobiidae) Copeia 1984 1984 235 238 10.2307/1445066 · DOI
  42. Presgraves DC Sex chromosomes and speciation in Drosophila Trends Genet 2008 24 336 343 10.1016/j.tig.2008.04.007 18514967 PMC2819171 · DOI
  43. Prowell DP Howard DJ Berlocher SH Sex linkage and speciation in Lepidoptera Endless forms: Species and speciation 1998 New York Oxford Univ Press 309 319
  44. Qvarnstrom A Bailey RI Speciation through evolution of sex-linked genes Heredity 2009 102 4 15 10.1038/hdy.2008.93 18781167 · DOI
  45. Reimchen TE Nosil P Variable predation regimes predict the evolution of sexual dimorphism in a population of threespine stickleback Evolution 2004 58 1274 1281 15266976
  46. Reinhold K Sex linkage among genes controlling sexually selected traits Behav Ecol Sociobiol 1998 44 1 7 10.1007/s002650050508 · DOI
  47. Roberts RB Ser JR Kocher TD Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes Science 2009 326 998 1001 10.1126/science.1174705 19797625 PMC3174268 · DOI
  48. Rokas A Abbot P Harnessing genomics for evolutionary insights Trends Ecol Evol 2009 24 192 200 10.1016/j.tree.2008.11.004 19201503 · DOI
  49. Rosa R Caetano-Filho M Shibatta OA Giuliano-Caetano L Cytotaxonomy in distinct populations in Hoplias aff. malabaricus (Characiformes, Erythrinidae) from lower Paranapanema River basin J Fish Biol 2009 75 2682 2694 10.1111/j.1095-8649.2009.02467.x 20738516 · DOI
  50. Ross JA Peichel CL Molecular cytogenetic evidence of rearrangements on the Y chromosome of the threespine stickleback fish Genetics 2008 179 2173 2182 10.1534/genetics.108.088559 18689886 PMC2516089 · DOI
  51. Ross JA Urton JR Boland J Shapiro MD Peichel CL Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae) PLoS Genet 2009 5 e1000391 10.1371/journal.pgen.1000391 19229325 PMC2638011 · DOI
  52. Saitoh K Multiple sex-chromosome system in a loach fish Cytogenet Cell Genet 1989 52 62 64 10.1159/000132840 2612215 · DOI
  53. Tanaka K Takehana Y Naruse K Hamaguchi S Sakaizumi M Evidence for different origins of sex chromosomes in closely related Oryzias fishes: substitution of the master sex-determining gene Genetics 2007 177 2075 2081 10.1534/genetics.107.075598 17947439 PMC2219477 · DOI
  54. Thorgaard GH Sex chromosomes in the sockeye salmon: a Y-autosome fusion Can J Genet Cytology 1978 20 349 354 570442
  55. Ueda T Ojima Y Sex chromosomes in the Kokanee salmon Oncorhynchus nerka Bull Jpn Soc Sci Fish 1984 50 1495 1498 10.2331/suisan.50.1495 · DOI
  56. Ueno K Ota K Kobayashi T Heteromorphic sex chromosomes of lizardfish (Synodontidae): focus on the ZZ-ZW1W2 system in Trachinocephalus myops Genetica 2001 111 133 142 10.1023/A:1013749027620 11841162 · DOI
  57. Ueno K Takai A Multiple sex chromosome system of X1X1X2X2/X1X2Y type in lutjanid fish, Lutjanus quinquelineatus (Perciformes) Genetica 2008 132 1 35 41 10.1007/s10709-007-9146-5 17351816 · DOI
  58. Uyeno T Miller RR Multiple sex chromosomes in a Mexican cyprinodontid fish Nature 1971 231 452 453 10.1038/231452a0 4931601 · DOI
  59. Uyeno T Miller RR Fitzsimons JM Karyology of the Cyprinodontoid fishes of the Mexican family Goodeidae Copeia 1983 1983 497 510 10.2307/1444395 · DOI
  60. van Doorn GS Kirkpatrick M Turnover of sex chromosomes induced by sexual conflict Nature 2007 449 909 912 10.1038/nature06178 17943130 · DOI
  61. White MJD Animal Cytology and Evolution 1973 Cambridge Cambridge Univ Press
  62. Woram RA Comparative genome analysis of the primary sex-determining locus in salmonid fishes Genome Res 2003 13 272 280 10.1101/gr.578503 12566405 PMC420375 · DOI
  63. Yamada M Higuchi M Goto A Extensive introgression of mitochondrial DNA found between two genetically divergent forms of threespine stickleback, Gasterosteus aculeatus, around Japan Environ Biol Fish 2001 61 269 284 10.1023/A:1010874117127 · DOI
  64. Yamada M Higuchi M Goto A Long-term occurrence of hybrids between Japan Sea and Pacific Ocean forms of threespine stickleback, Gasterosteus aculeatus, in Hokkaido Island, Japan Environ Biol Fish 2007 80 435 443 10.1007/s10641-006-9142-0 · DOI

Cited by

Sorted by citations

Authors
Kitano, J., & Peichel, C. L.
Affiliations
  • National Institute of Genetics (JP)
  • Fred Hutch Cancer Center (US)
Corresponding author
Kitano, Jun
ORCID
Venue
Environmental Biology of Fishes
Publisher
Springer Science and Business Media LLC
Published
2011-06-04
Volume
94
Issue
3
Pages
549-558
ISSN
  • 0378-1909 (ISSN-L)
  • 1573-5133
DOI
10.1007/s10641-011-9853-8
PMC
PMC4459657
OpenAlex
W2137006372
Cited by
178
References
0
Citations by year
2026: 8 · 2025: 13 · 2024: 14 · 2023: 10 · 2022: 13 · 2021: 10 · 2020: 18 · 2019: 18 · 2018: 8 · 2017: 9 · 2016: 12 · 2015: 9 · 2014: 25 · 2013: 9 · 2012: 1
FWCI
6.70
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • Environmental Biology of Fishes (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health
  • Japan Society for the Promotion of Science (22770075)
  • National Human Genome Research Institute (P50HG002568)
  • National Institute of General Medical Sciences (R01GM071854)
  • Precursory Research for Embryonic Science and Technology
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
Keywords
sex chromosome turnover, multiple sex chromosome system, neo-sex chromosomes, Gasterosteus aculeatus, speciation, reproductive isolation, phenotypic divergence, sympatric species pairs, Y chromosome evolution, fish

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review