The evolution of haploid chromosome numbers in Meliponini

Autoři: Natália Martins Travenzoli aff001;  Danon Clemes Cardoso aff002;  Hugo de Azevedo Werneck aff003;  Tânia Maria Fernandes-Salomão aff002;  Mara Garcia Tavares aff003;  Denilce Meneses Lopes aff001
Působiště autorů: Laboratório de Citogenética de Insetos, Departamento de Biologia Geral, Universidade Federal de Viçosa, CEP, Viçosa, Minas Gerais, Brazil aff001;  Laboratório de Genética Evolutiva e de Populações, Departamento de Biodiversidade, Evolução e Meio Ambiente, Universidade Federal de Ouro Preto, CEP, Ouro Preto, Minas Gerais, Brazil aff002;  Laboratório de Biologia Molecular de Insetos, Departamento de Biologia Geral, Universidade Federal de Viçosa, CEP, Viçosa, Minas Gerais, Brazil aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


It is thought that two evolutionary mechanisms gave rise to chromosomal variation in bees: the first one points to polyploidy as the main cause of chromosomal evolution, while the second, Minimum Interaction Theory (MIT), is more frequently used to explain chromosomal changes in Meliponini and suggests that centric fission is responsible for variations in karyotype. However, differences in chromosome number between Meliponini and its sister taxa and in the karyotype patterns of the Melipona genus cannot be explained by MIT, suggesting that other events were involved in chromosomal evolution. Thus, we assembled cytogenetical and molecular information to reconstruct an ancestral chromosome number for Meliponini and its sister group, Bombini, and propose a hypothesis to explain the evolutionary pathways underpinning chromosomal changes in Meliponini. We hypothesize that the common ancestor shared by the Meliponini and Bombini tribes possessed a chromosome number of n = 18. The karyotype with n = 17 chromosomes was maintained in Meliponini, and variations of haploid numbers possibly originated through additional Robertsonian fissions and fusions. Thus, the low chromosome number would not be an ancestral condition, as predicted by MIT. We then conclude that Robertsonian fission and fusions are unlikely to be the cause of chromosomal rearrangements that originated the current karyotypes in Meliponini.

Klíčová slova:

Bees – Cytogenetics – Heterochromatin – Chromosome structure and function – Karyotypes – Phylogenetic analysis – Phylogenetics – Sequence databases


1. Hoshiba H, Kusanagi A. Karyological study of honeybee. J Apic Res. 1978;17: 105–109.

2. Owen RE, Richardfs KW, Wilkes A. Chromosome numbers and karyotypic variation in Bumble bees (Hymenoptera: Apidae; Bombini). J Kans Entomol Soc. 1995;68: 290–302.

3. Hines HM, Cameron SA, Williams PH. Molecular phylogeny of the bumble bee subgenus Pyrobombus (Hymenoptera: Apidae: Bombus) with insights into gene utility for lower-level analysis. Invertebr Syst. 2006;20: 289–303.

4. Cameron SA, Hines HM, Williams PH. A comprehensive phylogeny of the bumble bees (Bombus). Biol J Linn Soc. 2007;91: 161–188.

5. Michener CD. The Bees of the World. The John Hopkins University Press, London. 2007.

6. Camargo JMF, Pedro SEM. Meliponini Lepeletier, 1836. In Moure J.S., Urban D., Melo G.A.R. (Orgs). Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region—online version. 2013. Available at Last Accessed 6/06/2018).

7. Rasmussen C, Cameron SA. Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biol J Linn Soc Lond. 2010;99: 206–232.

8. Fernandes A, Werneck HA, Pompolo SG, Lopes DM. Evidence of separate karyotype evolutionary pathway in Euglossa orchid bees by cytogenetic analyses. An Acad Bras Ciênc. 2013;85: 937–944. doi: 10.1590/S0001-37652013005000050 23969851

9. Françoso E, Oliveira FF, Arias MC. An interative approach identifies a new pecies of bumblebee (Hymenoptera: Apidae: Bombini) from northeastern Brazil. Apidologie.2016;47: 171–185.

10. Tavares MG, Lopes DM, Campos LAO. An overview of cytogenetics of the tribe Meliponine (Hymenoptera: Apidae). Genetica. 2017;145: 1–18. doi: 10.1007/s10709-016-9939-5

11. Hoshiba H, Imai HT. Chromosome evolution of bees and wasps (Hymenoptera, Apocrita) on the basis of C-banding pattern analyses. Jpn J Entomol. 1993;61: 465–492.

12. Cunha MS, Travenzoli NM, Ferreira RP, Cassinela EK, Silva H, Salomão TMF, et al. Comparative cytogenetics in three Melipona species (Hymenoptera: Apidae) with two divergent heterochromatic patterns. Genet Mol Biol. 2018;4: 806–813.

13. Cristiano MP, Simões TG, Lopes DM, das Graças Pompolo S. Cytogenetics of Melitoma segmentaria (Fabricius, 1804) (Hymenoptera, Apidae) reveals differences in the characteristics of heterochromatin in bees. Comp Cytogenet. 2014;8: 223. doi: 10.3897/CompCytogen.v8i3.7510 25349673

14. Brito RM, Pompolo SG, Magalhães MFM, Barros EG, Sakamoto-Hojo ET. Cytogenetic characterization of two Partamona species (Hymenoptera, Apidae, Meliponini) by fluorochrome staining and localization of 18 S rDNA clusters by FISH. Cytologia. 2005;70: 73–380.

15. Piccoli MCA, Bardella VB, Cabral-de-Mello DC. Repetitive DNAs in Melipona scutellaris (Hymenoptera: Apidae: Meliponidae): chromosomal distribution and test of multiple heterochromatin amplification in the genus. Apidologie. 2018;1: 8.

16. Kerr WE, Silveira ZV. Karyotypic evolution of bees and corresponding taxonomic implications. Evol Int J Org Evol. 1972;26: 197–202.

17. Imai HT. On the origin of telocentric chromosomes in Mammals. J Theor Biol. 1978;71: 619–637. doi: 10.1016/0022-5193(78)90328-4 661326

18. Imai HT, Maruyama T, Gojobori T, Inoue Y, Crozier RH. Theoretical bases for karyotype evolution. The minimum-interaction hypothesis. Am Nat. 1986;128: 900–920.

19. Imai HT, Taylor RW, Crosland MW, Crozier RH. Modes of spontaneous chromosomal mutation and karyotype evolution in ants with reference to the minimum interaction hypothesis. J Gen. 1988;63: 159–185.

20. Imai HT, Taylor RW, Crozier RH. Experimental bases for the minimum interaction theory. I. Chromosome evolution in ants of the Myrmecia pilosula species complex (Hymenoptera: Formicidae: Myrmeciinae). J Gen. 1994;69: 137–182.

21. Imai HT, Satta Y, Takahata N. Integrative study on chromosome evolution of mammals, ants and wasps based on the minimum interaction theory. J Theor Biol. 2001;210: 475–497. doi: 10.1006/jtbi.2001.2327 11403567

22. Costa KF, Brito RM, Miyazawa CS. Karyotypic description of four species of Trigona (Jurine, 1807) (Hymenoptera, Apidae, Meliponini) from the State of Mato Grosso, Brazil. Genet Mol Biol. 2004;27: 187–190.

23. Krinski D, Fernandes A, Rocha MP, Pompolo SDG. Karyotypic description of the stingless bee Oxytrigona cf. flaveola (Hymenoptera, Apidae, Meliponina) of a colony from Tangará da Serra, Mato Grosso State, Brazil. Genet Mol Biol. 2010;33: 494–498. doi: 10.1590/S1415-47572010000300020 21637423

24. Godoy DC, Ferreira RP, Lopes DM. Chromosomal variation and cytogenetics of Plebeia lucii and P. phrynostoma (Hymenoptera: Apidae). Fla Entomol. 2013;96: 1559–1566.

25. Rocha MP, Pompolo SG, Campos LAO. Citogenética da tribo Meliponini (Hymenoptera, Apidae). In: Melo GAR, Santos IA (eds) Apoidea Neotropica. 2003b. Homenagem aos 90 anos de Jesus Santiago Moure. UNESC, Santa Catarina.

26. Katoh K, Standley DM. MAFFT: iterative refinement and additional methods. Methods Mol Biol. 2014;1079: 131–146. doi: 10.1007/978-1-62703-646-7_8 24170399

27. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30: 2725–2729. doi: 10.1093/molbev/mst197 24132122

28. Tomita M, Shimizu N, Brutlag DL. Introns and Reading frames: correlation between splicing sites and their codon positions. Genome Biol Evol. 1996;13: 1219–1223.

29. Kawakita A, Sota T, Ascher JS, Ito M, Tanaka H, Kato M. Evolution and phylogenetic utility of alignment gaps within intron sequences of three nuclear genes in bumble bees (Bombus). Mol Biol Evol. 2003;20: 87–92. doi: 10.1093/molbev/msg007 12519910

30. Vaidya G, Lohman DJ, Meier R. Sequence Matrix: concatenation software for the fast assembly of multigene datasets with character set and codon information. Cladistics. 2011;27: 171–180.

31. Miller MA, Pfeiffer W, Schwartz T. "Creating the CIPRES Science Gateway for inference of large phylogenetic trees" in Proceedings of the Gateway Computing Environments Workshop (GCE). 2011. New Orleans, LA.

32. Ronquist F, Klopfstein S, Vilhelmsen L, Schulmeister S, Murray DL, Rasnitsyn AP. A total-evidence approach to dating with fossils, applied to the early radiation of the Hymenoptera. Syst Biol. 2012;61: 973–99. doi: 10.1093/sysbio/sys058 22723471

33. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatic. 2003;19: 1572–1574.

34. Rambaut A, Drummond A. Tracer, Version 1.7. 2009. Last accessed 22/08/2019.

35. Rambaut A. FigTree, ver. 1.3.1. [Online]. Available: figtree/. 2009. Last accessed 02/05/2018.

36. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, Xie D, et al. BEAST 2: A Software Platform for Bayesian Evolutionary Analysis. PLoS Comput Biol. 2014;10: e1003537. doi: 10.1371/journal.pcbi.1003537 24722319

37. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. Relaxed phylogenetics and dating with confidence. PloS Biol. 2006;4: 699–710.

38. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7: 214. doi: 10.1186/1471-2148-7-214 17996036

39. Martins AC, Melo GAR, Renner SS. The corbiculate bees arose from New World oil-collecting bees: Implications for the origin of pollen baskets. Mol Phylogenet Evol. 2014;80: 88–94. doi: 10.1016/j.ympev.2014.07.003 25034728

40. Madison WP, Madison DR. Mesquite: A modular system for evolutionary analysis, version 2.75. 2011. Last accessed 02/06/2018.

41. Glick L, Mayrose I. ChromEvol: Assessing the pattern of chromosome number evolution and the inference of polyploidy along a phylogeny. Mol Biol Evol. 2014;31: 1914–1922. doi: 10.1093/molbev/msu122 24710517

42. Cristiano MP, Cardoso DC, Fernandes-Salomao TM. Cytogenetic and molecular analyses reveal a divergence between Acromyrmex striatus (Roger, 1863) and other congeneric species: taxonomic implications. PloS One. 2013;8: 9.

43. Cardoso DC, Pompolo SG, Cristiano MP, Tavares MG. The role of fusion in ant chromosome evolution: insights from cytogenetic analysis using a molecular phylogenetic approach in the genus Mycetophylax. PLoS One. 2014;9: e87473. doi: 10.1371/journal.pone.0087473 24489918

44. Domingues AMT, Waldschmidt AM, Andrade SE, Andrade-Souza V, Alves RMDO, Silva-Junior JCD, et al. Karyotype characterization of Trigona fulviventris Guérin, 1835 (Hymenoptera, Meliponini) by C banding and fluorochrome staining: Report of a new chromosome number in the genus. Genet Mol Biol. 2005a;28: 390–393.

45. Francini IB, Gross MC, Nunes-Silva CG, Carvalho-Zilse GA. Cytogenetic analysis of the Amazon stingless bee Melipona seminigra merrillae reveals different chromosome number for the genus. Sci Agric. 2011;68: 592–593.

46. Lopes DM, Pompolo SDG, Campos LADO, Tavares MG. Cytogenetic characterization of Melipona rufiventris Lepeletier 1836 and Melipona mondury Smith 1863 (Hymenoptera, Apidae) by C banding and fluorochromes staining. Genet Mol Biol. 2008;31: 49–52.

47. Silva AA, Rocha MP. Karyotypic description of the stingless bee Melipona quinquefasciata Lepeletier, 1836 (Hymenoptera, Meliponini) with emphasis on the presence of B chromosomes. Comp Cytogenet. 2018;12: 471. doi: 10.3897/CompCytogen.v12i4.29165 30479700

48. Camacho JPM. B Chromosomes. The Evolution of the Genome. 2005; pp.223–286

49. Houben A, Banaei-Moghaddam AM, Klemme S, Timmis JN. Evolution and biology of supernumerary B chromosomes. Cell Mol Life Sci. 2014; 71: 467–478. doi: 10.1007/s00018-013-1437-7 23912901

50. Camacho JPM, Sharbel TF, Beukeboom LW. B-chromosome evolution. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences. 2000; 355: 163–178. doi: 10.1098/rstb.2000.0556 10724453

51. Anjos A, Rocha GC, Paladini A, Mariguela TC, Cabral-de-Mello DC. Karyotypes and repetitive DNA evolution in six species of the genus Mahanarva (Auchenorrhyncha: Cercopidae). Cytogenet Genome Res. 2016; 149: 321–327. doi: 10.1159/000450730 27811473

52. McAllister BF, Werren JH. Hybrid origin of a B chromosome (PSR) in the parasitic wasp Nasonia vitripennis. Chromosoma. 1996;106: 243–253.

53. Pompolo SG, Campos LAO. Karyotypes of two species of stingless bees, Leurotrigona muelleri and Leurotrigona pusilla (Hymenoptera, Meliponinae). Rev Bras Genet. 1995;18: 181–184.

54. Rocha MP, Pompolo SG. Karyotypes and heterochromatin variation (C-bands) in Melipona species (Hymenoptera, Apidae, Meliponinae). Genet Mol Biol. 1998;21: 41–45.

55. Rocha MP, Pompolo SG, Dergam JA, Fernandes A, Campos LAO. DNA characterization and karyotypic evolution in the bee genus Melipona (Hymenoptera, Meliponini). Hereditas. 2002;136: 19–27. doi: 10.1034/j.1601-5223.2002.1360104.x 12184485

56. Rocha MP, Cruz MP, Pompolo SG, Fernandes A, Silva JCJR, Waldschmidt AM. Longitudinal differentiation in Melipona mandacaia (Hymenoptera, Meliponini) chromosomes. Hereditas. 2003a;138: 133–137.

57. Barth A, Fernandes A, Pompolo SDG, Costa MA. Occurrence of B chromosomes in Tetragonisca Latreille, 1811 (Hymenoptera, Apidae, Meliponini): a new contribution to the cytotaxonomy of the genus. Genet Mol Biol. 2011;34: 77–79. doi: 10.1590/S1415-47572010005000100 21637547

58. Pompolo SG. Estudos citogenéticos em Meliponinae. Anais do Encontro Brasileiro sobre Biologia de Abelhas e outros Insetos Sociais. Naturalia. 1992. Ed. Especial, pp 62–66.

59. Costa MA, Pompolo SG, Campos LAO. Supernumerary chromosomes in Partamona cupira (Hymenoptera, Apidae, Meliponinae). Rev Bras Genet. 1992;15: 801–806.

60. Kerr WE. Estudos sobre o gênero Melipona. Na Esc Super Agric Luiz de Queiroz. 1948;5: 182–276.

61. Kerr WE, Nielsen RA. Evidence that genetically determined Melipona queens can become workers. Genetics. 1966;54: 859–865. 5970624

62. Rasmussen C, Cameron SA. A molecular phylogeny of the old word stingless bees (Hymenoptera: Apidae: Meliponini) and the non-monophyly of the large genus Trigona. Syst Entomol. 2007;32: 26–39.

63. Ramírez SR, Nieh JC, Quental TB, Roubik DW, Imperatriz-Fonseca VLI, Pierce NE. A molecular phylogeny of the stingless bee genus Melipona (Hymenoptera: Apidae). Mol Phylogenet Evol. 2010;56: 519–525. doi: 10.1016/j.ympev.2010.04.026 20433931

64. White MJD. Animal cytology and evolution. 1973. 3rd ed. Cambrige University Press.

65. Menezes RST, Carvalho JPSO, Silva TS, Somovilla A, Costa MA. Evolutionary trends in the chromosome numbers of swarm-founding social wasps. Insec Soc. 2014;61: 385–393.

66. Gokhman VE. Karyotype Evolution in Parasitic Wasps (Hymenoptera). Zool Zhurnal. 2004;83: 961–970.

67. Warchałowska-Śliwa E, Grzywacz B, Heller KG, Chobanov DP. Comparative analysis of chromosomes in the Palaearctic bush-crickets of tribe Pholidopterini (Orthoptera, Tettigoniinae). Comp Cytogenet. 2017;11: 309. doi: 10.3897/CompCytogen.v11i2.12070 28919967

68. Wang W, Lan H. Rapid and parallel chromosomal number reductions in muntjac deer inferred from mitochondrial DNA phylogeny. Mol Biol Evol. 2000;17: 1326–1333. doi: 10.1093/oxfordjournals.molbev.a026416 10958849

69. Hartmann N, Scherthan H. Characterization of ancestral chromosome fusion points in the Indian muntjac deer. Chromosoma. 2004;112: 213–220. doi: 10.1007/s00412-003-0262-4 14648169

70. Chi JX, Huang L, Nie W, Wang J, Su B, Yang F. Defining the orientation of the tandem fusions that occurred during the evolution of Indian muntjac chromosomes by BAC mapping. Chromosoma. 2005;114: 167–172. doi: 10.1007/s00412-005-0004-x 16010580

71. Tsipouri V, Schueler MG, Hu S, Dutra A, Pak E, Riethman H, et al. Comparative sequence analyses reveal sites of ancestral chromosomal fusions in the Indian muntjac genome. Genome Biol. 2008;9: R155. doi: 10.1186/gb-2008-9-10-r155 18957082

72. Imai HT, Crozier RH, Taylor RW. Karyotype evolution in Australian ants. Chromosoma. 1977;59: 341–393.

73. Busin CS, Vinciprova G, Recco-Pimentel SM. Chromosomal rearrangements as the source of variation in the number of chromosomes in Pseudis (Amphibia, Anura). Genetica. 2000;110: 131–141. doi: 10.1023/a:1017957716678 11678503

74. Primo CC, Glugoski L, Almeida MC, Zawadzki CH, Moreira-Filho O, Vicari MR, et al. Mechanisms of chromosomal diversification in species of Rineloricaria (Actinopterygii: Siluriformes: Loricariidae). Zebrafish. 2017;14: 161–168. doi: 10.1089/zeb.2016.1386 28027029

75. Robinson TJ, Ruiz-Herrera A, Froenicke L. Dissecting the mammalian genome–new insight into chromosomal evolution. Trends Genet. 2006;22: 297–301. doi: 10.1016/j.tig.2006.04.002 16678302

76. Andrade-Souza V, Duarte OMP, Martins CCC, Santos MGC, Costa MA. Comparative molecular cytogenetics of Melipona Illiger species (Hymenoptera: Apidae). Sociobiology. 2018;65: 696–705.

77. Kerr WE. Some aspects of the Evolution of social bees. Evol Biol. 1969;3: 119–175.

78. Kerr WE. Numbers of chromosomes in some species of bees. J Kansas Entomol Soc. 1972;45: 11–122.

79. Mampumbu AR. Análise citogenética da heterocromatina e da NOR em populações de abelhas sem ferrão Friesella schrottkyi (Friese, 1900) Hymenoptera: Apidae: Meliponini). Dissertation. Universidade Estadual de Campinas UNICAMP, Campinas, Brasil. 2002. Available from:

80. Nascimento S. Caracterização citogenética da espécie Frieseomelitta trichocerata Moure, 1988 (Hymenoptera; Apidae; Meliponina) coletada em Tangará da Serra-MT. Monography, Universidade do Estado de Mato Grosso. 2005.

81. Tarelho ZVS. Contribuição ao estudo citogenético dos Apoidea. Dissertation. Universidade de São Paulo, Ribeirão Preto. 1973.

82. Silveira ZV. Número de cromossomos em meliponídeos brasileiros. Ciênc Cult. 1971;23: 105–106.

83. Lopes DM, Fernandes A, Praça-Fontes MM, Werneck HA, Resende HC, Campos LAO. Cytogenetics of three Melipona species (Hymenoptera, Apidae, Meliponini). Sociobiology. 2011;58: 185–194.

84. Hoshiba H. Karyological analysis of a stingless bee, Melipona favosa (Apidae, Hymenoptera). Cytologia, 1988;53: 153–156.

85. Kerr WE, Araújo VP. Contribuição ao estudo citológico dos Apoidea. I. Espermatogênese em três espécies africanas. Garcia de Orta. 1957;3: 431–433.

86. Caixeiro AP. Caracterização citogenética da heterocromatina constitutiva e sua implicação na evolução do cariótipo de espécies do gênero Plebeia (Hymenoptera: Apinae: Meliponini). Dissertation. Universidade Federal de Viçosa. 1999. Available from:

87. Godoy DC, Lopes DM, Ferreira RP. Caracterização cariotípica de duas espécies de Meliponini da região Amazônica. In: Anais do Simpósio de Integração Acadêmica de 2014 da Universidade Federal de Viçosa. Viçosa, Minas Gerais. 2014.

88. Domingues AMT. Estudos citogenéticos comparativos entre espécies de Scaura (Hymenoptera, Apidae, Meliponini). Dissertation. Universidade Estadual de Santa Cruz. 2005b. Available from:

89. Waldschmidt AM, Duarte OMP, Martins CCC, Santana SEA, Miranda EA, Alves RNO, et al. Análises citogenéticas em espécies de abelhas da subtribo Meliponina (Hymenoptera: Meliponina) da região sudoeste da Bahia. In: Anais do 51° Congresso Brasileiro de Genética. Águas de Lindoia, São Paulo, p 253. 2005.

90. Ferreira RP. Análise citogenética de abelhas do gênero Trigona Jurine, 1807 (Hymenoptera, Meliponini). Thesis. Universidade Federal de Viçosa. 2015. Available from:

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden