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Issue: Vol. 5432 No. 1: 27 Mar. 2024
Type: Article
Published: 2024-03-27
DOI: 10.11646/zootaxa.5432.1.8
Page range: 109-120
Abstract views: 102
PDF downloaded: 3

A novel multiple sex chromosome system in Orthoptera, found in the tree cricket Oecanthus rubromaculatus Zefa, 2022 (Grylloidea, Oecanthidae)

Programa de Pós-Graduação em Biodiversidade Animal; Universidade Federal de Pelotas; Instituto de Biologia; Departamento de Ecologia; Zoologia e Genética; Campus Universitário Capão do Leão s/n; Capão do Leão; RS; Brazil.
Instituto de Desenvolvimento Sustentável Mamirauá; Tefé; Amazonas; Brazil.
Programa de Pós-Graduação em Biodiversidade Animal; Universidade Federal de Pelotas; Instituto de Biologia; Departamento de Ecologia; Zoologia e Genética; Campus Universitário Capão do Leão s/n; Capão do Leão; RS; Brazil.
Programa de Pós-Graduação em Biologia Animal; Universidade Federal do Rio Grande do Sul; Instituto de Biociências; Departamento de Genética; Campus do Vale; Av. Bento Gonçalves; 9500; Porto Alegre; RS; Brazil.
Programa de Pós-Graduação em Genética e Biologia Molecular; Universidade Federal do Rio Grande do Sul; Instituto de Biociências; Departamento de Genética; Campus do Vale; Av. Bento Gonçalves; 9500; Porto Alegre; RS; Brazil.
Programa de Pós-Graduação em Biodiversidade Animal; Universidade Federal de Pelotas; Instituto de Biologia; Departamento de Ecologia; Zoologia e Genética; Campus Universitário Capão do Leão s/n; Capão do Leão; RS; Brazil.
Universidade Estadual do Oeste do Paraná; Centro de Ciências Biológicas e da Saúde; Laboratório de Orthoptera; Rua Universitária; 2069; 858190-110; Cascavel; PR; Brazil.
Pontifícia Universidade Católica do Rio Grande do Sul; Faculdade de Biociências; Departamento de Biodiversidade e Ecologia; Laboratório de Entomologia; Av. Ipiranga; 6681; 90619-900; Porto Alegre; RS; Brazil.
Orthoptera Insect Ensifera karyotype meiosis cytogenetics

Abstract

The X0♂/XX♀ sex chromosome system prevails in most Orthopteran species. The X chromosome stands as one of the largest chromosomes within the complement, and is characterized by its heterochromatic nature. Variations of this model were found in some species of grasshoppers, crickets, and katydids, based on X/autosome rearrangements, giving rise to new sex chromosome systems, such as neo-XY♂/XX♀ and neo-X1X2Y♂/X1X1X2X2♀. The sex chromosome system neo-X1X20♂/X1X1X2X2♀ is rare in Orthoptera, and was observed only in two cricket species. In this study, we present the first multiple chiasmatic sex chromosome system in Orthoptera, found in the tree cricket Oecanthus rubromaculatus Zefa, 2022 from two distinct locations in the State of Rio Grande do Sul, Brazil. In one location, individuals exhibited a karyotype with 2n = 12, X1X2Y1Y2♂/X1X1X2X2♀, while in the other a karyotype of 2n = 12, X1X2X3Y1Y2Y3♂/X1X1X2X2X3X3♀ was observed. We proposed a model to explain the evolutionary steps in the formation of these karyotypes, based on chromosomal information of the Neotropical Oecanthus’ species. In this context, we proposed a hypothesis to explain the chromosome reorganization in O. rubromaculatus, starting from an ancestral karyotype of 2n = 21, X0♂, like the karyotype found in Oecanthus pictus Milach & Zefa, 2015, resulting in a significant reduction to 2n = 12 in O. rubromaculatus. This reorganization has led to the emergence of the novel multiple sex chromosome system in Orthoptera.

References

  1. Aswanianarayana, N.V. & Ashwath, S. (2005) Karyotype characteristics of forty-one species of Orthoptera and their evolutionary trends at the family level. Zoological Survey of India, 104, 157–164. https://doi.org/10.26515/rzsi/v104/i1-2/2005/159331
  2. Beaudry, J.R. (1973) Une analyse des complements chromosomiques de certains orthopteres du Quebec et sa signification taxonomique et evolutionnaire. Canadian Journal of Genetics and Cytology, 15 (1), 155–170. https://doi.org/10.1139/g73-016
  3. Bhattacharjee, T.K. & Manna, C.K. (1967) A cytological survey of Grylloidea. Proceeding 54th Indian Science Congress, 3, 420–421.
  4. Bidau, C., Martí, D.A. & Castillo, E.R. (2011) Inexorable spread: inexorable death? The fate of neo-XY chromosomes of grasshoppers. Journal of Genetics, 90 (3), 397–400. https://doi.org/10.1007/s12041-011-0108-4
  5. Blackmon, H., Ross, L. & Bachtrog, D. (2016) Sex determination, sex chromosomes, and karyotype evolution in insects. Journal of Heredity, 108, 78–93. https://doi.org/10.1093/jhered/esw047
  6. Campos, L.D., Souza-Dias, P.G.B., Audino, J.A., Desutter-Grandcolas, L. & Nihei, S.S. (2022) The fifth family of the true crickets (Insecta: Orthoptera: Ensifera: Grylloidea), Oecanthidae defin. nov.: phylogenetic relationships and divergence times. Zoological Journal of the Linnean Society, 197, 1034–1077. https://doi.org/10.1093/zoolinnean/zlac066
  7. Castillo, E.R.D., Martí, D.A. & Bidau, C.J. (2010) Sex and Neo-Sex chromosomes in Orthoptera: A Review. Journal of Orthoptera Research, 19 (2), 213–231. https://doi.org/10.1665/034.019.0207
  8. Castillo, E.R.D., Taffarel, A., Maronna, M.M, Cigliano, M.M., Palacios-Gimenez, O.M., Cabral-de-Mello, D.C. & Martí, D.A. (2017) Phylogeny and chromosomal diversification in the Dichroplus elongatus species group (Orthoptera, Melanoplinae). Plos One, 12, 1–22. https://doi.org/10.1371/journal.pone.0172352
  9. Castillo, E.R.D., Scattolini, M.C., Palacios-Gimenez, O.M., Martí, D.A. Cabral-De-Mello, D.C. & Cigliano, M.M. (2023) Karyotype evolution in Ronderosia grasshoppers (Orthoptera: Acrididae). Zoological Journal of the Linnean Society, 198(2), 351–367. https://doi.org/10.1093/zoolinnean/zlac090
  10. Charlesworth, D. (2017) Evolution of recombination rates between sex chromosomes. Philosophical Transactions of the Royal Society B, 372 (1736), 1–8. https://doi.org/10.1098/rstb.2016.0456
  11. Charlesworth, B. & Charlesworth, D. (2000) The degeneration of Y chromosomes. Philosophical Transactions of the Royal Society B, 355, 1563–1572. https://doi.org/10.1098/rstb.2000.0717
  12. Charlesworth, D., Charlesworth, B. & Marais, G. (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity, 95, 118–128. https://doi.org/10.1038/sj.hdy.6800697
  13. Cigliano, M.M., Braun, H., Eades, D.C. & Otte, D. (2024) Orthoptera Species File. Version 5.0/5.0. Available from: http://Orthoptera.SpeciesFile.org (accessed 20 February 2024)
  14. Das, N. & Das, R.C. (1991) Karyological studies of an Indian cricket Madasumma ventralis Walker (Orthoptera: Gryllidae). Caryologia: International Journal of Cytology, Cytosystematics and Cytogenetics, 44 (2), 209–215. https://doi.org/10.1080/00087114.1991.10797187
  15. Ferretti, A.B.S.M., Milani, D., Palacios-Gimenez, O.M., Ruiz-Ruano, F.J. & Cabral-de-Mello, D.C. (2020) High dynamism for neo-sex chromosomes: satellite DNAs reveal complex evolution in a grasshopper. Heredity, 125, 124–137. https://doi.org/10.1038/s41437-020-0327-7
  16. Frías, D. & Atria, J. (1998) Chromosomal variation, macroevolution and possible parapatric speciation in Mepraia spinolai (Porter) (Hemiptera: Reduviidae). Genetics and Molecular Biology, 21 (2), 179–184. https://doi.org/10.1590/s1415-47571998000200002
  17. Gazoni, T. &. Haddad, C.F.B., Narimatsu, H., Cabral-de-Mello, D.C., Lyra, M.L. & Parise-Maltempi, P.P. (2018) More sex chromosomes than autosomes in the Amazonian frog Leptodactylus pentadactylus. Chromosoma, 127, 269–278. https://doi.org/10.1007/s00412-018-0663-z
  18. Hewitt, G.M. (1979) Orthoptera: Grasshoppers and crickets. In: Jolui, B. (Ed.), Animal Cytogenetics 3. Insecta I. Gebrüder-Borntraeger, Berlin-Stuttgart, pp. 170.
  19. Husemann, M., Dey, L.‑S., Sadílek, D., Ueshima, N., Hawlitschek, O., Song, H. & Weissman, D.B. (2022) Evolution of chromosome number in grasshoppers (Orthoptera: Caelifera: Acrididae). Organisms Diversity & Evolution, 22, 649–657. https://doi.org/10.1007/s13127-022-00543-1
  20. Johnson, H.H. (1931) n.k. In: Centrioles and other cytoplasmic components of the male germ cells of the Gryllidae. Akad. Verlag Ges, Nova Iorque, pp. 116–162.
  21. Kaiser, V.B. & Bachtrog, D. (2010) Evolution of sex chromosomes in insects. Annual Review of Genetics, 44, 91–112. https://doi.org/10.1146/annurev-genet-102209-163600
  22. Kitada, S. (1949) Preliminary notes on the chromosomes of Oecanthus indicus. Kromosomo, 5 (6), 227–228.
  23. Levan, A., Fredga, K. & Sandberg, A.A. (1964) Nomenclature for centromeric position on chromosomes. Hereditas, 52 (2), 201–220. https://doi.org/10.1111/j.1601-5223.1964.tb01953.x
  24. Liebenberg, H., Fosseya, A. & Jacobsa, D.H. (1991) An unexpected sex chromosome mechanism in a South African mantid Polyspilota aeriginosa Goeza. Caryologia: International Journal of Cytology, Cytosystematics and Cytogenetics, 44 (2), 195–200. https://doi.org/10.1080/00087114.1991.10797185
  25. Lima, M.M. & Seuánez, H.N. (1991) Chromosome studies in the red howler monkey, Alouatta seniculus stramineus (Platyrrhini, Primates): description of an X1X2Y1Y2/X1X1X2X2 sex-chromosome system and karyological comparisons with other subspecies. Cytogenetic and Genome Research, 57 (2–3), 151–156. https://doi.org/10.1159/000133135
  26. Makino, S. (1932) An unequal pair of idiochromosomes in the tree cricket, Oecanthus longicauda. Journal of the Faculty of Science, Hokkaido University, Series VI, Zoology, 2 (1), 1–35.
  27. Manna, G.K. (1969) Some aspects of chromosome cytology. 56th Indian Science Congress Association, Proceeding Pt. II, 1–30.
  28. Martins, V.G. (1999) Karyotype evolution in the Termitidae (Isoptera). Sociobiology, 34 (3), 395–405.
  29. Martins, V.G. & Mesa, A. (1995) Two permanent linear chains of sex chromosomes in Neotermes fulvescens and karyotypes of two other neotropical Kalotermitidae species (Insecta, Isoptera). Genome, 38, 958–967. [http://hdl.handle.net/11449/66025] https://doi.org/10.1139/g95-126
  30. Mesa, A & Garcia-Novo, P. (2001) Neometrypus badius a new species of cricket with an unusual sex determining mechanism (Grylloidea, Eneopteridae, Tafaliscinae, Neometrypini). Journal of Orthoptera Research, 10 (1), 81–87. [https://www.jstor.org/stable/3503677] https://doi.org/10.1665/1082-6467(2001)010[0081:NBANSO]2.0.CO;2
  31. Mesa, A., Ferreira, A. & Carbonell, C.S. (1982) Cariologia de los acridiodeos neotropicales: estado actual de su conocimiento y nuevas contribuciones. Annales de la Société entomologique de France, 18, 507–526. https://doi.org/10.1080/21686351.1982.12278337
  32. Mesa, A., Fontanetti, C.S. & García-Novo, P. (2001) Does an x-autosome centric fusion in Acridoidea condemn the species to extinction? Journal of Orthoptera Research, 10 (2), 141–146. [https://www.jstor.org/stable/3503732] https://doi.org/10.1665/1082-6467(2001)010[0141:DAXACF]2.0.CO;2
  33. Mesa, A., García-Novo, P. & Santos, D. (2002) X1X2O (male) – X1X1X2X2 (female) chromosomal sex determining mechanism in the cricket Cicloptyloides americanus (Orthoptera, Grylloidea, Mogoplistidae). Journal of Orthoptera Research, 11 (1), 87–90. https://doi.org/10.1665/1082-6467(2002)011[0087:XXOMXX]2.0.CO;2
  34. Milach, E.M., Martins, L.P., Costa, M.K.M., Gottschalk, M.S., Oliveira, G.L., Redü, D.R., Neutzling, A.S., Dornelles, J.E.F., Vasconcellos, L.A. & Zefa, E. (2015) A new species of tree crickets Oecanthus (Orthoptera, Gryllidae, Oecanthinae) in tobacco plantation from Southern Brazil, with body color variation. Zootaxa, 4018 (2), 266–278. https://doi.org/10.11646/zootaxa.4018.2.6
  35. Milach, E.M., Costa, M.K.M., Martins, L.D.P., Nunes, L.A., Silva, D.S.M., Garcia, F.R.M., Oliveira, E.C. & Zefa, E. (2016) New species of tree cricket Oecanthus Serville, 1831 (Orthoptera: Gryllidae: Oecanthinae) from Reserva Natural Vale, Espírito Santo, Brazil, with chromosome complement. Zootaxa, 4173 (2), 137–146. https://doi.org/10.11646/zootaxa.5155.3.8
  36. Misof, B., Liu, S.L., Meusemann, K., Peters, R.S., Donath, A., Mayer, C., Frandsen, P.B., Ware, J., Flouri, T., Beutel, R.G., Niehuis, O., Petersen, M., Izquierdo-Carrasco, F., Wappler, T., Rust, J., Aberer, A.J., Aspöck, U., Aspöck, H., Bartel, D., Blanke, A., Berger, S., Böhm, A., Buckley, T.R., Calcott, B., Chen, J.Q., Friedrich, F., Fukui, M., Fujita, M., Greve, C., Grobe, P., Gu, S.C., Huang, Y., Jermiin, L.S., Kawahara, A.Y., Krogmann, L., Kubiak, M., Lanfear, R., Letsch, H., Li, Y.Y., Li, Z.Y., Li, J.G., Lu, H.R., Machida, R., Mashimo, Y., Kapli, P., McKenna, D.D., Meng, G.L., Nakagaki, Y., NavarreteHeredia, J.L., Ott, M., Ou, Y.X., Pass, G., Podsiadlowski, L., Pohl, H., von Reumont, B.M., Schütte, K., Sekiya, K., Shimizu, S., Slipinski, A., Stamatakis, A., Song, W.H., Su, X., Szucsich, N.U., Tan, M.H., Tan, X.M., Tang, M., Tang, J.B., Timelthaler, G., Tomizuka, S., Trautwein, M., Tong, X.L., Uchifune, T., Walzl, M.G., Wiegmann, B.M., Wilbrandt, J., Wipfler, B., Wong, T.K.F., Wu, Q., Wu, G.X., Xie, Y.L., Yang, S.Z,, Yang, Q., Yeates, D.K., Yoshizawa, K., Zhang, Q., Zhang, R., Zhang, W.W., Zhang, Y.H., Zhao, J., Zhou, C.R., Zhou, L.L., Ziesmann, T., Zou, S.J., Li, Y.R. Xu, X., Zhang, Y., Yang, H.M., Wang, J., Wang, J., Kjer, K.M. & Zhou, X. (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science, 346, 763–767. https://doi.org/10.1126/science.1257570
  37. Nakamura, K. & Kitada, J.I. (1955) Chromosomes of some orthopteroid insects, with special reference to sex-chromosomes. Cytologia, 20 (2), 119–132. https://doi.org/10.1508/cytologia.20.119
  38. Ohmachi, F. (1927) Preliminary note on cytological studies on Gryllodea: chromosome numbers and sex chromosome of eighteen species. Proceedings of the Imperial Academy of Japan, 3, 451–456. https://doi.org/10.2183/pjab1912.3.451
  39. Ohmachi, F. (1935) Comparative study of chromosome complements in the Gryllodea in relation to taxonomy. Bulletin of Mie Imperial College of Agriculture and Forestry, 5, 1–48.
  40. Ohmachi, F. (1951) A list of the chromosome numbers in the Grylloidea. Tsue, 1951, 1–6.
  41. Palacios-Gimenez, O.M., Castillo, E.R.D., Martí, D.A. & Cabral-de-Mello, D.C. (2013) Tracking the evolution of sex chromosome systems in Melanoplinae grasshoppers through chromosomal mapping of repetitive DNA sequences. BMC Evolutionary Biology, 13 (167), 1–12. https://doi.org/10.1186/1471-2148-13-167
  42. Palacios-Gimenez, O.M., Marti, D.A. & Cabral-de-Mello, D.C. (2015) Neo-sex chromosomes of Ronderosia bergi: insight into the evolution of sex chromosomes in grasshoppers. Chromosoma, 124, 353–365. https://doi.org/10.1007/s00412-015-0505-1
  43. Raychaudhuri, S.P. & Manna, G.K. (1950) Evidence of a multiple sex-chromosome mechanism in a gryllid. Journal of Heredity, 41, 277–280. https://doi.org/10.1093/oxfordjournals.jhered.a106057
  44. Rice, W.R. (1996) Evolution of the Y sex chromosome in animals. Bioscience, 46, 331–343. https://doi.org/10.2307/1312947
  45. Rodrigues, N., Vueille, Y., Brelsford, B.A., Merilä, J. & Perrin, N. (2016) The genetic contribution to sex determination and number of sex chromosomes varies among populations of common frogs (Rana temporaria). Heredity, 117 (1), 25–32. https://doi.org/10.1038/hdy.2016.22
  46. Saez, F.A. (1963) Gradient of heterochromatinization in the evolution of the sexual system “neo-X neo-Y”. Portugaliae Acta Biologica, Series A, 7, 111–138.
  47. Sassi, F.M.C, Sember, A., Deon, G.A., Liehr, T., Padutsch, N., Oyakawa, O.T., Vicari, M.R., Bertollo, L.A.C., Moreira‑Filho, O. & Cioffi, M.B. (2023) Homeology of sex chromosomes in Amazonian Harttia armored catfishes supports the X‑fission hypothesis for the X1X2Y sex chromosome system origin. Scientific Reports—Nature, 13, 15756. https://doi.org/10.1038/s41598-023-42617-w
  48. Sember, A., Nguyen, P., Perez, M.F., Altmanová, M., Ráb, P. & Cioffi, M.B. (2021) Multiple sex chromosomes in teleost fishes from a cytogenetic perspective: state of the art and future challenges. Philosophical Transactions of the Royal Society B, 376, 20200098. https://doi.org/10.1098/rstb.2020.0098
  49. Sharov, A.G. (1968) The phylogeny of the Orthopteroidea. Trudy Paleontologicheskogo Instituta Akademii Nauk, 118, 1–213. [English translation 1971]
  50. Silva, A.F., Oliveira, T.D., Bertocchi, N.A., Valente, V.L.S., Zefa, E. & Deprá, M. (2022) Study of four Neotropical species of tree crickets Oecanthus Serville, 1831 (Orthoptera, Gryllidae) using cytogenetic and molecular markers. Genetics and Molecular Biology, 45 (2), 1–12. https://doi.org/10.1590/1678-4685-GMB-2021-0213
  51. Solari, A.J. & Rahn, M.I. (2005) Fine structure and meiotic behavior of the male multiple sex chromosomes in the genus Alouatta. Cytogenetic and Genome Research, 108, 262–267. https://doi.org/10.1159/000080825
  52. Smith, S.G. (1953) A pseudo-multiple sex-chromosome mechanism in an Indian Gryllid. Chromosoma, 5, 555–573. https://doi.org/10.1007/BF01271502
  53. Timm, V.T., Martins, L.P., Acosta, R.C., Szinwelski, N., Pereira, M.R., Costa, M.K.M. & Zefa, E. (2021) Trends of karyotype evolution in the Neotropical long-legged crickets Phalangopsidae (Orthoptera, Grylloidea). Zootaxa, 4938 (1), 101–116. https://doi.org/10.11646/zootaxa.4938.1.5
  54. Warchalowska-Śliva, E. (1998) Karyotype characteristics of katydid Orthopterans (Ensifera, Tettigoniidae), and remarks on their evolution at different taxonomic levels. Folia Biologica, 46 (3), 143–176.
  55. Warchałowska-Śliwa, E., Grzywacz, B., Maryańska-Nadachowska, A., Hemp, A. & Hemp, C. (2014) Different steps in the evolution of neo-sex chromosomes in two East African Spalacomimus species (Orthoptera: Tettigoniidae: Hetrodinae). European Journal of Entomology, 112 (1), 1–10. https://doi.org/10.14411/eje.2015.024
  56. White, M.J.D. (1954) Animal cytology and evolution. 2nd Edition. Cambridge University Press, London, 454 pp.
  57. White, M.J.D. (1973) Animal cytology and evolution. 3rd Edition. Cambridge University Press, London, 961 pp.
  58. Zefa, E., Acosta, R.C., Timm, V.F., Szinwelski, N., Marinho, M.A.T. & Costa, M.K.M. (2018) The Tree Cricket Neoxabea brevipes Rehn, 1913 (Orthoptera: Gryllidae: Oecanthinae) from the Brazilian southern Atlantic Forest: Morphology, bioacoustics, and cytogenetics. Zootaxa, 4531 (4), 554–566. https://doi.org/10.11646/zootaxa.4531.4.6
  59. Zefa, E., Acosta, R.C., Timm, V.F. & Costa, M.K.M. (2022) New species of tree cricket Oecanthus Serville, 1831 (Orthoptera: Grylloidea) from Southern Brazilian Atlantic Forest, with bioacoustics. Zootaxa, 5155 (3), 439–448. https://doi.org/10.11646/zootaxa.5155.3.8
  60. Zefa, E., Redu, D.R., Costa, M.K.M., Gottschalk, M.S., Padilha, G.B., Silva, A.F. & Martins, L.P. (2014) A new species of Endecous Saussure, 1878 (Orthoptera, Gryllidae) from northeast Brazil with the first X1X20 chromosomal sex system in Gryllidae. Zootaxa, 3847 (1), 125–132. https://doi.org/10.11646/zootaxa.3847.1.7