Tempo and mode in karyotype evolution revealed by a probabilistic model incorporating both chromosome number and morphology
Autoři:
Kohta Yoshida aff001; Jun Kitano aff001
Působiště autorů:
Ecological Genetics Laboratory, National Institute of Genetics, Mishima, Japan
aff001
Vyšlo v časopise:
Tempo and mode in karyotype evolution revealed by a probabilistic model incorporating both chromosome number and morphology. PLoS Genet 17(4): e1009502. doi:10.1371/journal.pgen.1009502
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009502
Souhrn
Karyotype, including the chromosome and arm numbers, is a fundamental genetic characteristic of all organisms and has long been used as a species-diagnostic character. Additionally, karyotype evolution plays an important role in divergent adaptation and speciation. Centric fusion and fission change chromosome numbers, whereas the intra-chromosomal movement of the centromere, such as pericentric inversion, changes arm numbers. A probabilistic model simultaneously incorporating both chromosome and arm numbers has not been established. Here, we built a probabilistic model of karyotype evolution based on the “karyograph”, which treats karyotype evolution as a walk on the two-dimensional space representing the chromosome and arm numbers. This model enables analysis of the stationary distribution with a stable karyotype for any given parameter. After evaluating their performance using simulated data, we applied our model to two large taxonomic groups of fish, Eurypterygii and series Otophysi, to perform maximum likelihood estimation of the transition rates and reconstruct the evolutionary history of karyotypes. The two taxa significantly differed in the evolution of arm number. The inclusion of speciation and extinction rates demonstrated possibly high extinction rates in species with karyotypes other than the most typical karyotype in both groups. Finally, we made a model including polyploidization rates and applied it to a small plant group. Thus, the use of this probabilistic model can contribute to a better understanding of tempo and mode in karyotype evolution and its possible role in speciation and extinction.
Klíčová slova:
Animal phylogenetics – Centromeres – Evolutionary rate – Karyotypes – Phylogenetic analysis – Polyploidy – Speciation – Species extinction
Zdroje
1. Stebbins GL. Chromosomal Evolution in Higher Plants. London: Edward Arnold; 1971.
2. White MJD. Animal Cytology and Evolution. Cambridge: Cambridge University Press; 1973.
3. King M. Species Evolution: the Role of Chromosome Change. Cambdrige: Cambridge University Press; 1993.
4. Ratomponirina C, Brun B, Rumpler Y. Synaptonemal complexes in Robertsonian translocation heterozygous in lemurs. In: Brandham PE, editor. Kew Chromosome Conference III. London: HMSO Publications Center; 1988. p. 65–73.
5. White MJD. Modes of Speciation. San Francisco: W. H. Freeman and Company; 1978.
6. Rieseberg LH. Chromosomal rearrangements and speciation. Trends in Ecology and Evolution. 2001;16:351–8. doi: 10.1016/s0169-5347(01)02187-5 11403867
7. Guerrero RF, Kirkpatrick M. Local adaptation and the evolution of chromosome fusions. Evolution. 2014;68(10):2747–56. doi: 10.1111/evo.12481 24964074
8. Chambers SM. Rates of evolution in chromosome numbers in snails and vertebrates. Evolution. 1987;41(1):166–75. doi: 10.1111/j.1558-5646.1987.tb05779.x 28563768
9. Bush GL, Case SM, Wilson AC, Patton JL. Rapid speciation and chromosomal evolution in mammals. Proceedings of the National Academy of Sciences. 1977;74(9):3942. doi: 10.1073/pnas.74.9.3942 269445
10. Wilson AC, Sarich VM, Maxson LR. The importance of gene rearrangement in evolution: evidence from studies on rates of chromosomal, protein, and anatomical evolution. Proceedings of the National Academy of Sciences of the United States of America. 1974;71(8):3028–30. doi: 10.1073/pnas.71.8.3028 4528784
11. Glick L, Mayrose I. ChromEvol: assessing the pattern of chromosome number evolution and the inference of polyploidy along a phylogeny. Molecular Biology and Evolution. 2014;31(7):1914–22. doi: 10.1093/molbev/msu122 24710517
12. Mayrose I, Barker MS, Otto SP. Probabilistic models of chromosome number evolution and the inference of polyploidy. Systematic Biology. 2009;59(2):132–44. doi: 10.1093/sysbio/syp083 20525626
13. Hipp AL. Nonuniform processes of chromosome evolution in sedges (Carex: Cyperaceae). Evolution. 2007;61(9):2175–94. doi: 10.1111/j.1558-5646.2007.00183.x 17767589
14. Olmo E. Rate of chromosome changes and speciation in reptiles. Genetica. 2005;125(0016–6707 (Print)):185–203. doi: 10.1007/s10709-005-8008-2 16247691
15. Leaché AA-O, Banbury BL, Linkem CW, de Oca AN. Phylogenomics of a rapid radiation: is chromosomal evolution linked to increased diversification in north american spiny lizards (Genus Sceloporus)? BMC Evolutionary Biology. 2016;16(1471–2148 (Electronic)):63. doi: 10.1186/s12862-016-0628-x 27000803
16. Jones K. Robertsonian fusion and centric fission in karyotype evolution of higher plants. The Botanical Review. 1998;64:273–89.
17. Nachman MW, Searle JB. Why is the house mouse karyotype so variable? Trends in Ecology & Evolution. 1995;10:397–402. doi: 10.1016/s0169-5347(00)89155-7 21237083
18. Imai HT, Crozier RH. Quantitative analysis of directionality in mammalian karyotype evolution. The American Naturalist. 1980;116(4):537–69. doi: 10.1086/283646 29519129
19. Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R. Centromere repositioning in mammals. Heredity. 2012;108(1):59–67. doi: 10.1038/hdy.2011.101 22045381
20. Schubert I. What is behind "centromere repositioning"? Chromosoma. 2018;127:229–34. doi: 10.1007/s00412-018-0672-y 29705818
21. Pardo-Manuel de Villena F, Sapienza C. Female meiosis drives karyotypic evolution in mammals. Genetics. 2001;159:1179–89. 11729161
22. Imai HT, Maruyama T, Crozier RH. Rates of mammalian karyotype evolution by the karyograph method. The American Naturalist. 1983;121(4):477–88.
23. Eschmeyer WN, Fong JD. Species by family/subfamily in the Catalog of Fishes. California Academy of Sciences. 2016.
24. Galetti PM Jr., Aguilar CT, Molina WF. An overview of marine fish cytogenetics. Hydrobiologia. 2000;420:55–62.
25. Mank JE, Avise JC. Phylogenetic conservation of chromosome numbers in Actinopterygiian fishes. Genetica. 2006;127:321–7. doi: 10.1007/s10709-005-5248-0 16850236
26. FitzJohn RG. Diversitree: comparative phylogenetic analyses of diversification in R. Methods in Ecology and Evolution. 2012;3(6):1084–92.
27. Lukhtanov VA, Kandul NP, Plotkin JB, Dantchenko AV, Haig D, Pierce NE. Reinforcement of pre-zygotic isolation and karyotype evolution in Agrodiaetus butterflies. Nature. 2005;436(7049):385–9. doi: 10.1038/nature03704 16034417
28. Escudero M, Hipp AL, Luceño M. Karyotype stability and predictors of chromosome number variation in sedges: A study in Carex section Spirostachyae (Cyperaceae). Molecular Phylogenetics and Evolution. 2010;57(1):353–63. doi: 10.1016/j.ympev.2010.07.009 20655386
29. Schaeffer SW. Muller “Elements” in Drosophila: how the search for the genetic basis for. 451 speciation led to the birth of comparative genomics. Genetics. 2018;210(1):3–13. doi: 10.1534/genetics.118.301084 30166445
30. Blackmon H, Justison J, Mayrose I, Goldberg EE. Meiotic drive shapes rates of karyotype evolution in mammals. Evolution. 2019;73(3):511–23. doi: 10.1111/evo.13682 30690715
31. Kai W, Nomura K, Fujiwara A, Nakamura Y, Yasuike M, Ojima N, et al. A ddRAD-based genetic map and its integration with the genome assembly of Japanese eel (Anguilla japonica) provides insights into genome evolution after the teleost-specific genome duplication. BMC Genomics. 2014;15(1):233. doi: 10.1186/1471-2164-15-233 24669946
32. Kasahara M, Naruse K, Sasaki S, Nakatani Y, Qu W, Ahsan B, et al. The medaka draft genome and insights into vertebrate genome evolution. Nature. 2007;447(7145):714–9. doi: 10.1038/nature05846 17554307
33. Lysak MA, Mandáková T, Schranz ME. Comparative paleogenomics of crucifers: ancestral genomic blocks revisited. Current Opinion in Plant Biology. 2016;30:108–15. doi: 10.1016/j.pbi.2016.02.001 26945766
34. Lysak MA, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I. Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(13):5224. doi: 10.1073/pnas.0510791103 16549785
35. Murat F, Louis A, Maumus F, Armero A, Cooke R, Quesneville H, et al. Understanding Brassicaceae evolution through ancestral genome reconstruction. Genome Biology. 2015;16(1):262. doi: 10.1186/s13059-015-0814-y 26653025
36. Yoshida K, Kitano J. The contribution of female meiotic drive to the evolution of neo-sex chromosomes. Evolution. 2012;66:3198–208. doi: 10.1111/j.1558-5646.2012.01681.x 23025609
37. Barra V, Fachinetti D. The dark side of centromeres: types, causes and consequences of structural abnormalities implicating centromeric DNA. Nature Communications. 2018;9(1):4340. doi: 10.1038/s41467-018-06545-y 30337534
38. Fishman L, Willis JH, Wu CA, Lee YW. Comparative linkage maps suggest that fission, not polyploidy, underlies near-doubling of chromosome number within monkeyflowers (Mimulus; Phrymaceae). Heredity. 2014;112(5):562–8. doi: 10.1038/hdy.2013.143 24398885
39. Schubert I. Chromosome evolution. Current Opinion in Plant Biology. 2007;10(109–115). doi: 10.1016/j.pbi.2007.01.001 17289425
40. White MJD. Chromosomal rearrangements and speciation in animals. Annual Review of Genetics. 1969;3(1):75–98.
41. Novitski E. Non-random disjunction in Drosophila. Annual Review of Genetics. 1967;1(1):71–86.
42. Wilby AS, Parker JS. The supernumerary segment systems of Rumex acetosa. Heredity. 1988;60(1):109–17.
43. van Heemert C. Somatic pairing and meiotic nonrandom disjunction in a pericentric inversion of Hylemya antiqua (Meigen). Chromosoma. 977;59:193–206.
44. Foster GG, Whitten MJ. Meiotic drive in Lucilia cuprina and chromosomal evolution. The American Naturalist. 1991;137:403–15.
45. Coyne JA. A test of the role of meiotic drive in fixing a pericentric inversion. Genetics. 1989;123(1):241–3. 2806886
46. Schubert I, Oud JL. There is an upper limit of chromosome size for normal development of an organism. Cell. 1997;88(4):515–20. doi: 10.1016/s0092-8674(00)81891-7 9038342
47. Schubert I. Alteration of chromosome numbers by generation of minichromosomes–is there a lower limit of chromosome size for stable segregation?. Cytogenetics and Cell Genetics. 2001;93:175–81. doi: 10.1159/000056981 11528109
48. Rabosky DL, Goldberg EE. Model inadequacy and mistaken inferences of trait-dependent speciation. Systematic Biology. 2015;64(2):340–55. doi: 10.1093/sysbio/syu131 25601943
49. Louca S, Pennell MW. Extant timetrees are consistent with a myriad of diversification histories. Nature. 2020;580(7804):502–5. doi: 10.1038/s41586-020-2176-1 32322065
50. Arai R. Fish Karyotypes: A Check List. Tokyo: Springer Japan; 2011.
51. Nelson JS. Fishes of the World. New Jersey: Wiley; 2006.
52. Near TJ, Eytan RI, Dornburg A, Kuhn KL, Moore JA, Davis MP, et al. Resolution of ray-finned fish phylogeny and timing of diversification. Proceedings of the National Academy of Sciences. 2012;109(34):13698. doi: 10.1073/pnas.1206625109 22869754
53. Near TJ, Dornburg A, Eytan RI, Keck BP, Smith WL, Kuhn KL, et al. Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes. Proceedings of the National Academy of Sciences. 2013;110(31):12738. doi: 10.1073/pnas.1304661110 23858462
54. Yoshida K, Kitano J. Tempo and mode in karyotype evolution revealed by a probabilistic model incorporating both chromosome number and morphology [Data set] 2021 https://doi.org/10.5061/dryad.s4mw6m966
55. Pagel M. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society of London Series B: Biological Sciences. 1994;255(1342):37–45.
56. Rabosky DL, Santini F, Eastman J, Smith SA, Sidlauskas B, Chang J, et al. Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nature Communications. 2013;4(1):1958. doi: 10.1038/ncomms2958 23739623
57. Beilstein MA, Nagalingum NS, Clements MD, Manchester SR, Mathews S. Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proceedings of the National Academy of Sciences. 2010;107(43):18724. doi: 10.1073/pnas.0909766107 20921408
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