Chromosome number evolves at equal rates in holocentric and monocentric clades


Autoři: Sarah N. Ruckman aff001;  Michelle M. Jonika aff001;  Claudio Casola aff002;  Heath Blackmon aff001
Působiště autorů: Department of Biology, Texas A&M University, Texas, United States of America aff001;  Ecology and Evolutionary Biology Interdisciplinary Program, Texas A&M University, Texas, United States of America aff002;  Genetics Interdisciplinary Program, Texas A&M University, Texas, United States of America aff003;  Department of Ecology and Conservation Biology, Texas A&M, Texas, United States of America aff004
Vyšlo v časopise: Chromosome number evolves at equal rates in holocentric and monocentric clades. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009076
Kategorie: Research Article
doi: 10.1371/journal.pgen.1009076

Souhrn

Despite the fundamental role of centromeres two different types are observed across plants and animals. Monocentric chromosomes possess a single region that function as the centromere while in holocentric chromosomes centromere activity is spread across the entire chromosome. Proper segregation may fail in species with monocentric chromosomes after a fusion or fission, which may lead to chromosomes with no centromere or multiple centromeres. In contrast, species with holocentric chromosomes should still be able to safely segregate chromosomes after fusion or fission. This along with the observation of high chromosome number in some holocentric clades has led to the hypothesis that holocentricity leads to higher rates of chromosome number evolution. To test for differences in rates of chromosome number evolution between these systems, we analyzed data from 4,393 species of insects in a phylogenetic framework. We found that insect orders exhibit striking differences in rates of fissions, fusions, and polyploidy. However, across all insects we found no evidence that holocentric clades have higher rates of fissions, fusions, or polyploidy than monocentric clades. Our results suggest that holocentricity alone does not lead to higher rates of chromosome number changes. Instead, we suggest that other co-evolving traits must explain striking differences between clades.

Klíčová slova:

Animal evolution – Centromeres – Evolutionary rate – Chromosome structure and function – Insects – Phylogenetic analysis – Phylogenetics – Polyploidy


Zdroje

1. Wilson AC, Bush GL, Case SM, King MC. Social structuring of mammalian populations and rate of chromosomal evolution. Proceedings of the National Academy of Sciences. 1975;72(12):5061–5.

2. White MJD. Modes of speciation. San Francisco:: WH Freeman; 1978. 455 p.

3. Bush GL. What do we really know about speciation? Perspectives on evolution. 1982:119–31.

4. Escudero M, Hahn M, Brown BH, Lueders K, Hipp AL. Chromosomal rearrangements in holocentric organisms lead to reproductive isolation by hybrid dysfunction: The correlation between karyotype rearrangements and germination rates in sedges. American journal of botany. 2016;103(8):1529–36. doi: 10.3732/ajb.1600051 27558707

5. 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

6. Blackmon H, Ross L, Bachtrog D. Sex Determination, Sex Chromosomes, and Karyotype Evolution in Insects. Journal of Heredity. 2017;108(1):78–93. doi: 10.1093/jhered/esw047 27543823

7. Petitpierre E. Why beetles have strikingly different rates of chromosomal evolution. Elytron. 1987;1:25–32.

8. Faria R, Navarro A. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends in ecology & evolution. 2010;25(11):660–9.

9. Guerrero RF, Kirkpatrick M. Local Adaptation and the Evolution of Chromosome Fusions. Evolution. 2014.

10. Rieseberg LH. Chromosomal rearrangements and specieation. Trends Ecol Evol. 2001;16(7):351–8. doi: 10.1016/s0169-5347(01)02187-5 11403867

11. Lucek K. Evolutionary mechanisms of varying chromosome numbers in the radiation of Erebia butterflies. Genes. 2018;9(3):166.

12. Garagna S, Broccoli D, Redi CA, Searle JB, Cooke HJ, Capanna E. Robertsonian metacentrics of the house mouse lose telomeric sequences but retain some minor satellite DNA in the pericentromeric area. Chromosoma. 1995;103(10):685–92. doi: 10.1007/BF00344229 7664615

13. Miga KH. Chromosome-specific centromere sequences provide an estimate of the ancestral chromosome 2 fusion event in hominin genomes. Journal of Heredity. 2017;108(1):45–52. doi: 10.1093/jhered/esw039 27423248

14. Moretti A, Sabato S. Karyotype evolution by centromeric fission inZamia (Cycadales). Plant Systematics and Evolution. 1984;146(3–4):215–23.

15. Harlan JR, deWet JM. On Ö. Winge and a prayer: the origins of polyploidy. The botanical review. 1975;41(4):361–90.

16. Torres EM, Williams BR, Amon A. Aneuploidy: cells losing their balance. Genetics. 2008;179(2):737–46. doi: 10.1534/genetics.108.090878 18558649

17. Matsumoto T, Kitano J. The intricate relationship between sexually antagonistic selection and the evolution of sex chromosome fusions. Journal of theoretical biology. 2016;404:97–108. doi: 10.1016/j.jtbi.2016.05.036 27259387

18. Pennell MW, Kirkpatrick M, Otto SP, Vamosi JC, Peichel CL, Valenzuela N, et al. Y fuse? Sex chromosome fusions in fishes and reptiles. PLoS genetics. 2015;11(5):e1005237. doi: 10.1371/journal.pgen.1005237 25993542

19. Hill J, Rastas P, Hornett EA, Neethiraj R, Clark N, Morehouse N, et al. Unprecedented reorganization of holocentric chromosomes provides insights into the enigma of lepidopteran chromosome evolution. Science advances. 2019;5(6):eaau3648. doi: 10.1126/sciadv.aau3648 31206013

20. Lukhtanov VA, Dincă V, Friberg M, Šíchová J, Olofsson M, Vila R, et al. Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids. Proceedings of the National Academy of Sciences. 2018;115(41):E9610–E9.

21. Melters DP, Paliulis LV, Korf IF, Chan SW. Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Research. 2012;20(5):579–93. doi: 10.1007/s10577-012-9292-1 22766638

22. Mola L, Papeschi A. Holokinetic chromosomes at a glance. BAG-Journal of Basic and Applied Genetics. 2006;17(1):17–33.

23. Luceño M, Guerra M. Numerical variations in species exhibiting holocentric chromosomes: a nomenclatural proposal. Caryologia. 1996;49(3–4):301–9.

24. Malheiros-Garde N, Gardé A. Fragmentation as a possible evolutionary process in the genus Luzula DC. Genetica Iberica. 1950;2:257–62.

25. Faulkner J. Chromosome studies on Carex section Acutae in north-west Europe. Botanical Journal of the Linnean Society. 1972;65(3):271–301.

26. Cope T, editor Cytology and hybridization in the Juncus bufonius L. aggregate in western Europe. Watsonia; 1985: Citeseer.

27. Escudero M, Hipp AL, Hansen TF, Voje KL, Luceño M. Selection and inertia in the evolution of holocentric chromosomes in sedges (Carex, Cyperaceae). New Phytologist. 2012;195(1):237–47. doi: 10.1111/j.1469-8137.2012.04137.x 22489934

28. Schneider MC, Zacaro AA, Pinto-da-Rocha R, Candido DM, Cella DM. Complex meiotic configuration of the holocentric chromosomes: the intriguing case of the scorpion Tityus bahiensis. Chromosome Research. 2009;17(7):883–98. doi: 10.1007/s10577-009-9076-4 19760509

29. Panzera F, Pérez R, Hornos S, Panzera Y, Cestau R, Delgado V, et al. Chromosome numbers in the Triatominae (Hemiptera-Reduviidae): a review. Memórias do Instituto Oswaldo Cruz. 1996;91(4):515–8. doi: 10.1590/s0074-02761996000400021 9070413

30. Mora C, Tittensor DP, Adl S, Simpson AG, Worm B. How many species are there on Earth and in the ocean? PLoS biology. 2011;9(8).

31. Ross L, Blackmon H, Lorite P, Gokhman VE, Hardy NB. Recombination, chromosome number and eusociality in the Hymenoptera. Journal of evolutionary biology. 2015;28(1):105–16. doi: 10.1111/jeb.12543 25382409

32. Vershinina AO, Lukhtanov VA. Evolutionary mechanisms of runaway chromosome number change in Agrodiaetus butterflies. Scientific reports. 2017;7(1):1–9. doi: 10.1038/s41598-016-0028-x 28127051

33. Cook LG. Extraordinary and extensive karyotypic variation: a 48-fold range in chromosome number in the gall-inducing scale insect Apiomorpha (Hemiptera: Coccoidea: Eriococcidae). Genome. 2000;43(2):255–63. 10791813

34. Church SH, Donoughe S, de Medeiros BA, Extavour CG. Insect egg size and shape evolve with ecology but not developmental rate. Nature. 2019;571(7763):58–62. doi: 10.1038/s41586-019-1302-4 31270484

35. Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, et al. Phylogenomics resolves the timing and pattern of insect evolution. Science. 2014;346(6210):763–7. doi: 10.1126/science.1257570 25378627

36. Rainford JL, Hofreiter M, Nicholson DB, Mayhew PJ. Phylogenetic distribution of extant richness suggests metamorphosis is a key innovation driving diversification in insects. PLoS One. 2014;9(10).

37. FitzJohn RG. Diversitree: comparative phylogenetic analyses of diversification in R. Methods in Ecology and Evolution. 2012;3(6):1084–92.

38. Team RC. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria2020.

39. Robinson R. Lepidoptera genetics. Oxford: Pergamon Press; 1971.

40. Chmátal L, Gabriel SI, Mitsainas GP, Martínez-Vargas J, Ventura J, Searle JB, et al. Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Current Biology. 2014;24(19):2295–300. doi: 10.1016/j.cub.2014.08.017 25242031

41. Gassmann R, Rechtsteiner A, Yuen KW, Muroyama A, Egelhofer T, Gaydos L, et al. An inverse relationship to germline transcription defines centromeric chromatin in C. elegans. Nature. 2012;484(7395):534–7. doi: 10.1038/nature10973 22495302

42. Li Z, Tiley GP, Galuska SR, Reardon CR, Kidder TI, Rundell RJ, et al. Multiple large-scale gene and genome duplications during the evolution of hexapods. Proceedings of the National Academy of Sciences. 2018;115(18):4713–8.

43. Li Z, Tiley GP, Rundell RJ, Barker MS. Reply to Nakatani and McLysaght: analyzing deep duplication events. Proceedings of the National Academy of Sciences. 2019;116(6):1819–20.

44. Kandul NP, Lukhtanov VA, Pierce NE. Karyotypic diversity and speciation in Agrodiaetus butterflies. Evolution. 2007;61(3):546–59. doi: 10.1111/j.1558-5646.2007.00046.x 17348919

45. Nakatani Y, McLysaght A. Macrosynteny analysis shows the absence of ancient whole-genome duplication in lepidopteran insects. Proceedings of the National Academy of Sciences. 2019;116(6):1816–8.

46. 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

47. Mayrose I, Barker MS, Otto SP. Probabilistic models of chromosome number evolution and the inference of polyploidy. Systematic biology. 2010;59(2):132–44. doi: 10.1093/sysbio/syp083 20525626

48. Zenil-Ferguson R, Ponciano JM, Burleigh JG. Testing the association of phenotypes with polyploidy: An example using herbaceous and woody eudicots. Evolution. 2017;71(5):1138–48. doi: 10.1111/evo.13226 28295270

49. Poggio M, Bressa M, Papeschi A. Karyotype evolution in Reduviidae (Insecta: Heteroptera) with special reference to Stenopodainae and Harpactorinae. Comparative Cytogenetics. 2007;1(2):159–68.

50. White M, Key K, André M, Cheney J. Cytogenetics of the viatica group of morabine grasshoppers II. Kangaroo Island populations. Australian Journal of Zoology. 1969;17(2):313–28.

51. Lande R. The expected fixation rate of chromosomal inversions. Evolution. 1984:743–52. doi: 10.1111/j.1558-5646.1984.tb00347.x 28555823

52. Bengtsson BO. Rates of karyotype evolution in placental mammals. Hereditas. 1980;92:37–47. doi: 10.1111/j.1601-5223.1980.tb01676.x 6991455

53. 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):3942–6.

54. Imai HT, Maruyama T, Crozier RH. Rates of Mammalian Karyotype Evolution by the Karyograph Method. The American Naturalist. 1983;121(4):477–88.

55. Larson A, Prager EM, Wilson AC. Chromosomal evolution, speciation and morphological change in vertebrates: the role of social behaviour. Chromosomes Today. 1984;8:215–28.

56. Coyne JA. Correlation between heterozygosity and rate of chromosome evolution in animals. The American Naturalist. 1984;123(5):725–9.


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