#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Y Fuse? Sex Chromosome Fusions in Fishes and Reptiles


Chromosome number is a basic feature of the eukaryotic genome that has important consequences for recombination, segregation, and other processes. Despite a century of research on the evolution of karyotype, however, we still have little understanding of the evolutionary forces that enable chromosomal fusions and fissions to become established. Here, we compare the rates of chromosomal fusions between sex chromosomes (X, Y, Z, and W chromosomes) and autosomes. We find that these fusions more frequently involve the Y chromosome than other sex chromosomes in fishes and squamate reptiles. To account for these observations, we conduct theoretical analyses and find that the most likely explanation for this pattern is that fusions have deleterious effects, and further that mutation rates and/or sex ratios are biased. Improving our knowledge of the evolutionary mechanisms driving sex chromosome-autosome fusions provides a richer understanding of the forces that shape chromosomes generally.


Vyšlo v časopise: Y Fuse? Sex Chromosome Fusions in Fishes and Reptiles. PLoS Genet 11(5): e32767. doi:10.1371/journal.pgen.1005237
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005237

Souhrn

Chromosome number is a basic feature of the eukaryotic genome that has important consequences for recombination, segregation, and other processes. Despite a century of research on the evolution of karyotype, however, we still have little understanding of the evolutionary forces that enable chromosomal fusions and fissions to become established. Here, we compare the rates of chromosomal fusions between sex chromosomes (X, Y, Z, and W chromosomes) and autosomes. We find that these fusions more frequently involve the Y chromosome than other sex chromosomes in fishes and squamate reptiles. To account for these observations, we conduct theoretical analyses and find that the most likely explanation for this pattern is that fusions have deleterious effects, and further that mutation rates and/or sex ratios are biased. Improving our knowledge of the evolutionary mechanisms driving sex chromosome-autosome fusions provides a richer understanding of the forces that shape chromosomes generally.


Zdroje

1. King M (1993) Species evolution: the role of chromosome change. Cambdrige: Cambridge University Press.

2. White MJD (1973) Animal cytology and evolution. Cambridge: Cambridge University Press.

3. Chang S-L, Lai H-Y, Tung S-Y, Leu J-Y (2013) Dynamic large-scale chromosomal rearrangements fuel rapid adaptation in yeast populations. PLoS Genet 9: e1003232. doi: 10.1371/journal.pgen.1003232 23358723

4. Hou J, Friedrich A, de Montigny J, Schacherer J (2014) Chromosomal rearrangements as a major mechanism in the onset of reproductive isolation in Saccharomyces cerevisiae. Curr Biol 24: 1153–1159. doi: 10.1016/j.cub.2014.03.063 24814147

5. Pérez-Ortín JE, Querol A, Puig S, Barrio E (2002) Molecular characterization of a chromosomal rearrangement involved in the adaptive evolution of yeast strains. Genome Res 12: 1533–1539. 12368245

6. Schubert I, Lysak MA (2011) Interpretation of karyotype evolution should consider chromosome structural constraints. Trends Genet 27: 207–216. doi: 10.1016/j.tig.2011.03.004 21592609

7. Nachman MW, Searle JB (1995) Why is the house mouse karyotype so variable? Trends Ecol Evol 10: 397–402. 21237083

8. Guerrero RF, Kirkpatrick M (2014) Local adaptation and the evolution of chromosome fusions. Evolution 68: 2747–2756. doi: 10.1111/evo.12481 24964074

9. Charlesworth B, Coyne JA, Barton NH (1987) The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130: 113–146.

10. Bachtrog D, Kirkpatrick M, Mank JE, McDaniel SF, Pires JC, et al. (2011) Are all sex chromosomes created equal? Trends Genet 27: 350–357. doi: 10.1016/j.tig.2011.05.005 21962970

11. Beukeboom LW, Perrin N (2014) The evolution of sex determination. Oxford: Oxford University Press.

12. Ellegren H (2011) Sex-chromosome evolution: recent progress and the influence of male and female heterogamety. Nat Rev Genet 12: 257–266.

13. Bull JJ (1983) Evolution of sex determining mechanisms. Menlo Park: The Benjamin/Cummings Publishing Company.

14. Ezaz T, Stiglec R, Veyrunes F, Marshall Graves JA (2006) Relationships between vertebrate ZW and XY sex chromosome systems. Curr Biol 16: R736–R743. 16950100

15. Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, et al. (2014) Sex determination: why so many ways of doing it? PLoS Biol 12: e1001899. doi: 10.1371/journal.pbio.1001899 24983465

16. Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208: 191–364.

17. The Tree of Sex Consortium (2014) Tree of Sex: a datbase of sexual systems. Sci Data 1: 140015.

18. Ohno S (1967) Sex chromosomes and sex-linked genes. New York: Springer.

19. Ezaz T, Sarre SD, O’Meally D, Marshall Graves JA, Georges A (2009) Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenet Genome Res 127: 249–260. doi: 10.1159/000300507 20332599

20. Kitano J, Peichel CL (2012) Turnover of sex chromosomes and speciation in fishes. Environ Biol Fish 94: 549–558.

21. Yoshida K, Kitano J (2012) The contribution of female meiotic drive to the evolution of neo-sex chromosomes. Evolution 66: 3198–3208. doi: 10.1111/j.1558-5646.2012.01681.x 23025609

22. Maddison WP, Leduc-Robert G (2013) Multiple origins of sex chromosome fusions correlated with chiasma localization in Habronattus jumping spiders (Araneae: Salticidae). Evolution 67: 2258–2272. doi: 10.1111/evo.12109 23888849

23. Gardner RJM, Sutherland GR, Shaffer LG (2012) Chromosome abnormalities and genetic counseling. New York: Oxford University Press.

24. Dobigny G, Ozouf-Costaz C, Bonillo C, Volobouev V (2004) Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study. Chromosoma 113: 34–41. 15243753

25. Charlesworth D, Charlesworth B (1980) Sex differences in fitness and selection for centric fusions between sex-chromosomes and autosomes. Genet Res 35: 205–214. 6930353

26. Pardo-Manuel de Villena F, Sapienza C (2001) Female meiosis drives karyotypic evolution in mammals. Genetics 159: 1179–1189. 11729161

27. Pardo-Manuel de Villena F, Sapienza C (2001) Nonrandom segregation during meiosis: the unfairness of females. Mamm Genome 12: 331–339. 11331939

28. Searle JB (1986) Preferential transmission in wild common shrews (Sorex araneus), heterozygous for Robertsonian rearrangements. Genet Res 47: 147–148. 3710161

29. Wyttenbach A, Borodin P, Hausser J (1998) Meiotic drive favors Robertsonian metacentric chromosomes in the common shrew (Sorex araneus, Insectivora, Mammalia). Cytogenet Genome Res 83: 199–206.

30. Thomas NS, Morris JK, Baptista J, Ng BL, Crolla JA, et al. (2010) De novo apparently balanced translocations in man are predominantly paternal in origin and associated with a significant increase in paternal age. J Med Genet 47: 112–115. doi: 10.1136/jmg.2009.069716 19638350

31. Grossmann V, Höckner M, Karmous-Benailly H, Liang D, Puttinger R, et al. (2010) Parental origin of apparently balanced de novo complex chromosomal rearrangements investigated by microdissection, whole genome amplification, and microsatellite-mediated haplotype analysis. Clin Genet 78: 548–553. doi: 10.1111/j.1399-0004.2010.01419.x 20584030

32. Batista DS, Tuck-Muller C, Martinez J, Kearns W, Pearson P, et al. (1993) A complex chromosomal rearrangement detected prenatally and studied by fluorescence in situ hybridization. Hum Genet 92: 117–121. 8370575

33. Sartorelli EMP, Mazzucatto LF, de Pina-Neto JoM (2001) Effect of paternal age on human sperm chromosomes. Fertil Steril 76: 1119–1123. 11730737

34. Wyrobek AJ, Eskenazi B, Young S, Arnheim N, Tiemann-Boege I, et al. (2006) Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm. Proc Natl Acad Sci USA 103: 9601–9606. 16766665

35. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2: 349–368. 18103134

36. Bachtrog D (2008) The temporal dynamics of processes underlying Y chromosome degeneration. Genetics 179: 1513–1525. doi: 10.1534/genetics.107.084012 18562655

37. Clark AG (1988) The evolution of the Y chromosome with X-Y recombination. Genetics 119: 711–720. 3402733

38. Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95: 118–128. 15931241

39. Mank JE (2012) Small but mighty: the evolutionary dynamics of W and Y sex chromosomes. Chromosome Res 20: 21–33. doi: 10.1007/s10577-011-9251-2 22038285

40. Bandyopadhyay R, Heller A, Knox-DuBois C, McCaskill C, Berend SA, et al. (2002) Parental origin and timing of de novo Robertsonian translocation formation. Am J Hum Genet 71: 1456–1462. 12424707

41. Chamberlin J, Magenis RE (1980) Parental origin of de novo chromosome rearrangements. Hum Genet 53: 343–347. 6445322

42. van Doorn GS, Kirkpatrick M (2007) Turnover of sex chromosomes induced by sexual conflict. Nature 449: 909–912. 17943130

43. van Doorn GS, Kirkpatrick M (2010) Transitions between male and female heterogamety caused by sex-antagonistic selection. Genetics 186: 629–645. doi: 10.1534/genetics.110.118596 20628036

44. Charlesworth B, Wall JD (1999) Inbreeding, heterozygote advantage and the evolution of neo-X and neo-Y sex chromosomes. Proc R Soc Lond B 266: 51–56.

45. Rabosky DL, Santini F, Eastman J, Smith SA, Sidlauskas B, et al. (2013) Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nat Commun 4: 1958. doi: 10.1038/ncomms2958 23739623

46. Pyron RA, Burbrink FT (2014) Early origin of viviparity and multiple reversions to oviparity in squamate reptiles. Ecol Lett 17: 13–21. doi: 10.1111/ele.12168 23953272

47. Pyron RA, Burbrink FT, Wiens JJ (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 13: 93. doi: 10.1186/1471-2148-13-93 23627680

48. Pagel M (1994) Detecting correlated evolution on phylogenies: a general method for comparative analysis of discrete characters. Proc R Soc Lond B 255: 37–45.

49. FitzJohn RG (2012) Diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol Evol 3: 1084–1092.

50. Bertollo LAC, Oliveira C, Molina WF, Margarido VP, Fontes MS, et al. (2004) Chromosome evolution in the erythrinid fish, Erythrinus erythrinus (Teleostei: Characiformes). Heredity 93: 228–233. 15241446

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 5
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#