Abstract
Satellite DNAs (satDNAs) and transposable elements (TEs) are among the main components of constitutive heterochromatin (c-heterochromatin) and are related to their functionality, dynamics, and evolution. A peculiar case regarding the quantity and distribution of c-heterochromatin is observed in the genus of bees, Melipona, with species having a low amount of heterochromatin and species with high amount occupying almost all chromosomes. By combining low-pass genome sequencing and chromosomal analysis, we characterized the satDNAs and TEs of Melipona quadrifasciata (low c-heterochromatin) and Melipona scutellaris (high low c-heterochromatin) to understand c-heterochromatin composition and evolution. We identified 15 satDNA families and 20 TEs for both species. Significant variations in the repeat landscapes were observed between the species. In M. quadrifasciata, the repetitive fraction corresponded to only 3.78% of the genome library studied, whereas in M. scutellaris, it represented 54.95%. Massive quantitative and qualitative changes contributed to the differential amplification of c-heterochromatin, mainly due to the amplification of exclusive repetitions in M. scutellaris, as the satDNA MscuSat01-195 and the TE LTR/Gypsy_1 that represent 38.20 and 14.4% of its genome, respectively. The amplification of these two repeats is evident at the chromosomal level, with observation of their occurrence on most c-heterochromatin. Moreover, we detected repeats shared between species, revealing that they experienced mainly quantitative variations and varied in the organization on chromosomes and evolutionary patterns. Together, our data allow the discussion of patterns of evolution of repetitive DNAs and c-heterochromatin that occurred in a short period of time, after separation of the Michmelia and Melipona subgenera.
Similar content being viewed by others
References
Alvarez-Fuster A, Juan C, Petitpierre E (1991) Genome size in Tribolium flour beetles: inter-and intraspecific variation. Genetics Res 58:1–5. https://doi.org/10.1017/S0016672300029542
Allshire RC, Madhani HD (2018) Ten principles of heterochromatin formation and function. Nat Rev Mol Cell Biol 19:229. https://doi.org/10.1038/nrm.2017.119
Bao W, Kojima KK, Kohany O (2015) Repbase Update, a database of repetitive elements in eukaryotic genomes. Mob DNA 6:1–6. https://doi.org/10.1186/s13100-015-0041-9
Blommaert J (2020) Genome size evolution: towards new model systems for old questions. Proc R Soc B 287:20201441. https://doi.org/10.1098/rspb.2020.1441
Bourque G, Burns KH, Gehring M, Gorbunova V, Seluanov A, Hammell M, Imbeault M, Izsvák Z, Levin HL, Macfarlan ST, Mager LD, Feschotte C (2018) Ten things you should know about transposable elements. Genome Biol 19:1–12. https://doi.org/10.1186/s13059-018-1577-z
Cabral-de-Mello DC, Marec F (2021) Protocolo de hibridização in situ de fluorescência universal (FISH) para mapear DNAs repetitivos em insetos e outros artrópodes. Mol Genet Genomics 296:513–526. https://doi.org/10.1007/s00438-021-01765-2
Camargo JMF, Pedro SRM (2013) 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. Available at http://www.moure.cria.org.br/catalogue. Accessed 10 Aug 2020.
Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220. https://doi.org/10.1038/371215a0
Christmas MJ, Wallberg A, Bunikis I, Olsson A, Wallerman O, Webster MT (2019) Chromosomal inversions associated with environmental adaptation in honey-bees. Mol Ecol 28:1358–1374. https://doi.org/10.1111/mec.1494
Cunha MSD, Travenzoli NM, Ferreira RDP, Cassinela EK, Silva HBD, Oliveira FPM, Salomão TMF, Lopes DM (2018) Comparative cytogenetics in three Melipona species (Hymenoptera: Apidae) with two divergent heterochromatic patterns. Genet Mol Biol 41:806–813. https://doi.org/10.1590/1678-4685-GMB-2017-0330
Cunha MS, Campos LAO, Lopes DM (2020) Insights into the heterochromatin evolution in the genus Melipona (Apidae: Meliponini). Insect Soc 67:391–398. https://doi.org/10.1007/s00040-020-00773-6
Díez CM, Gaut BS, Meca E, Scheinvar E, Montes-Hernandez S, Eguiarte LE, Tenaillon MI (2013) Genome size variation in wild and cultivated maize along altitudinal gradients. New Phytol 199:264–276. https://doi.org/10.1111/nph.12247
Dover GA (1982) Molecular drive: a cohesive mode of species evolution. Nature 199:111–117. https://doi.org/10.1016/0168-9525(86)90211-8
Drummond A, Ashton B, Cheung M, Heled J, Kearse M, Moir R, Stones-Havas S, Thierer T, Wilson S. (2009) Geneious v4.8. http://geneious.com. Accessed 19 Aug 2019
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: uma nova série de programas para realizar análises genéticas de populações em Linux e Windows. Mol Ecol Resour 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Feliciello I, Akrap I, Brajković J, Zlatar I, Ugarković Đ (2015) Satellite DNA as a driver of population divergence in the red flour beetle Tribolium castaneum. Genome Biol Evol 7:228–239. https://doi.org/10.1093/gbe/evu280
Ferree PM, Barbash DA (2009) Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol 7:e1000234. https://doi.org/10.1371/journal.pbio.1000234
Fry K, Salser W (1977) Nucleotide sequence of HS-a satellite DNA from kangaroo rat Dipodomys ordii and characterisation of similar sequences in other rodents. Cell 12:1069–1084. https://doi.org/10.1016/0092-8674(77)90170-2
Garrido-Ramos MA (2017) Satellite DNA: an Evolving Topic Genes 8:230. https://doi.org/10.3390/genes8090230
Gregory TR (2021) Animal genome size database. http://www.genomesize.com. Accessed 20 Apr 2021
Imai HT, Taylor RW, Crosland MW, Crozier RH (1988) Modes of spontaneous chromosomal mutation and karyotype evolution in ants with reference to the minimum interaction hypothesis. Jpn J Appl Entomol Z 63:159–185. https://doi.org/10.1266/jjg.63.159
Klein SJ, O’Neill RJ (2018) Transposable elements: genome innovation, chromosome diversity, and centromere conflict. Chromosom Res 26:5–23. https://doi.org/10.1007/s10577-017-9569-5
Liu J, Ali M, Zhou Q (2020) Establishment and evolution of heterochromatin. Ann N Y Acad Sci 1476:59–77. https://doi.org/10.1111/nyas.14303
Landais I, Chavigny P, Castagnone C, Pizzol J, Abad P, Vanlerberghe-Masutti F (2000) Characterization of a highly conserved satellite DNA from the parasitoid wasp Trichogramma brassicae. Gene 255:65–73. https://doi.org/10.1016/S0378-1119(00)00318-8
Lopes DM, Pompolo SDG, Campos LADO, Tavares MG (2008) Cytogenetic characterization of Melipona rufiventris Lepeletier 1836 and Melipona mondury Smith 1863 (Hymenoptera, Apidae) by C banding and fluorochromes staining. Genet Mol Biol 31:49–52. https://doi.org/10.1590/S1415-47572008000100010
Lopes DM, Fernandes A, Praça-Fontes MM, Werneck HDA, Resende HC, Campos LADO (2011) Cytogenetics of three Melipona species (Hymenoptera, Apidae, Meliponini). Sociobiology 58:185–194
López-Flores I, Garrido-Ramos MM (2012) The repetitive DNA content of eukaryotic genomes. Cytogenet Genome Res 7:1–28. https://doi.org/10.1159/000337118
Meštrović N, Castagnone-Sereno P, Plohl M (2006) High conservation of the differentially amplified MPA2 satellite DNA family in parthenogenetic root-knot nematodes. Gene 376:260–267. https://doi.org/10.1016/j.gene.2006.04.008
Michener CD (2007) The Bees of the World. The John Hopkins, 2nd Ed. University Press, Baltimore. pp953
Novák P, Neumann P, Pech J, Steinhaisl J, Macas J (2013) RepeatExplorer: a Galaxy-based web server for genomewide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29:792–793. https://doi.org/10.1093/bioinformatics/btt054
Palacios-Gimenez OM, Milani D, Song H et al (2020) Eight million years of satellite DNA evolution in grasshoppers of the genus Schistocerca illuminate the ins and outs of the library hypothesis. Genome Biol Evol 12:88–102. https://doi.org/10.1093/gbe/evaa018
Pereira JA, Travenzoli NM, de Oliveira MP, de Azevedo WH, Salomão TMF, Lopes DM (2021) Molecular cytogenetics in the study of repetitive sequences helping to understand the evolution of heterochromatin in Melipona (Hymenoptera, Meliponini). Genetica 149:55–62. https://doi.org/10.1007/s10709-020-00111-5
Piccoli MCA, Bardella VB, Cabral-de-Mello DC (2018) Repetitive DNAs in Melipona scutellaris (Hymenoptera: Apidae: Meliponidae): chromosomal distribution and test of multiple heterochromatin amplification in the genus. Apidologie 49:497–504. https://doi.org/10.1007/s13592-018-0577-z
Plohl M, Meštrović N, Mravinac B (2012) Satellite DNA evolution. Genome 7:126–152. https://doi.org/10.1159/000337122
Ramírez SR, Nieh JC, Quental TB, Roubik DW, Imperatriz-Fonseca VL, Pierce NE (2010) A molecular phylogeny of the stingless bee genus Melipona (Hymenoptera: Apidae). Mol Phylogenet Evol 56:519–525. https://doi.org/10.1016/j.ympev.2010.04.026
Ricci M, Luchetti A, Bonandin L, Mantovani B (2013) Random DNA libraries from three species of the stick insect genus Bacillus (Insecta: Phasmida): repetitive DNA characterization and first observation of polyneopteran MITEs. Genome 56:729–735. https://doi.org/10.1139/gen-2013-0107
Rocha MP, Pompolo SG (1998) Karyotypes and heterochromatin variation (C-bands) in Melipona species (Hymenoptera, Apidae, Meliponinae). Genet Mol Biol 21:41–45. https://doi.org/10.1590/S1415-47571998000100008
Rocha MP, Pompolo SG, Dergam JA, Fernandes A, Campos LAO (2002) DNA characterization and karyotypic evolution in the bee genus Melipona (Hymenoptera Meliponini). Hereditas 136:19–27. https://doi.org/10.1034/j.1601-5223.2002.1360104.x
Rocha MP, Cruz MP, Fernandes A, Waldschmidt AM, Silva JC, Pompolo SG (2003) Longitudinal differentiation in Melipona mandacaia (Hymenoptera, Meliponini) cromossomes. Hereditas 138:133–137. https://doi.org/10.1034/j.1601-5223.2003.01699.x
Ruiz-Ruano FJ, López-León MD, Cabrero J, Camacho JPM (2016) High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep 6:28333. https://doi.org/10.1038/srep28333
Salser W, Bowen S, Browne D, El-Adli F, Fedoroff N, Fry K, Heidell H, Paddock G, Wallace B, Whitcome P (1976) Investigation of the organization of mammalian chromosomes at the DNA sequences level. Fed Proc 35:23–35
Silva AA, Rocha MP, Pompolo SG, Campos LAO, Tavares MG (2018) Karyotypic description of the stingless bee Melipona quinquefasciata Lepeletier, 1836 (Hymenoptera, Meliponini) with emphasis on the presence of B chromosomes. Comp Cytogenet 12:471–482. https://doi.org/10.3897/CompCytogen.v12i4.29165
Skinner BM, Griffin DK (2012) Intrachromosomal rearrangements in avian genome evolution: evidence for regions prone to break-points. Heredity 108:37–41. https://doi.org/10.1038/hdy.2011.99
Smit AFA, Hubley R, Green P (2017) RepeatMasker Open-4.0. http://www.repeatmasker.org
Stelzer CP, Pichler M, Stadler P, Hatheuer A, Riss S (2019) Within-population genome size variation is mediated by multiple genomic elements that segregate independently during meiosis. Genome Biol Evol 11:3424–3435. https://doi.org/10.1093/gbe/evz253
Tavares MG, Carvalho CR, Soares FAF (2010) Genome size variation in Melipona species (Hymenoptera: Apidae) and sub-grouping by their DNA content. Apidologie 41:636–642. https://doi.org/10.1051/apido/20010023
Travenzoli NM, Lima BA, Cardoso DC, Dergam JA, Fernandes-Salomão TM, Lopes DM (2019) Cytogenetic analysis and chromosomal mapping of repetitive DNA in Melipona species (Hymenoptera, Meliponini). Cytogenet Genome Res 158:213–224. https://doi.org/10.1159/000501754
Wei KHC, Grenier JK, Barbash DA, Clark AG (2014) Correlated variation and population differentiation in satellite DNA abundance among lines of Drosophila melanogaster. Proc Natl Acad Sci 111:18793–18798. https://doi.org/10.1073/pnas.1421951112
Wei KHC, Lower SE, Caldas IV, Sless TJ, Barbash DA, Clark AG (2018) Variable rates of simple satellite gains across the Drosophila phylogeny. Mol Biol Evol 35:925–941. https://doi.org/10.1093/molbev/msy005
Acknowledgements
We acknowledge the anonymous reviewers for the suggestions and manuscript improvement.
Funding
The authors would like to thank the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP), process number 2019/19069–7. DCC-d-M is a recipient of a research productivity fellowship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq (process number 308290/2020–8). VBB and ABSMF are supported by FAPESP, processes numbers 2018/21772–5 and 2020/06188–5, respectively.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
412_2021_764_MOESM1_ESM.docx
Supplementary Table S1 List of primers used for amplification through PCR of satDNAs and TEs from Melipona genomic DNAs. (DOCX 14 KB)
412_2021_764_MOESM2_ESM.docx
Supplementary Table S2 List of satDNA and TEs used for fluorescence in situ hybridization (FISH) mapping on chromosomes of MQUA and MSCU. Chromosome location: location of signals on chromosomes, P – pericentromeric, I – interstitial, D – dispersed, T – terminal, A – one chromosome arm, eu – euchromatin, het – heterochromatin. (DOCX 16 KB)
412_2021_764_MOESM3_ESM.jpg
Supplementary Figure 1 Comparative landscapes (abundance versus divergence) for the satDNAs shared between the genome of both species. Repeat element divergence in the K2P model distance to consensus is shown on the x-axis and the satDNA abundance on the y-axis. (a-c) satDNAs with more abundance of copies in the MSCU genome, and (d-h) more abundance of copies in the MQUA genome. (JPG 1101 KB)
412_2021_764_MOESM4_ESM.jpg
Supplementary Figure 2 Comparative landscapes (abundance versus divergence) for the TEs. Repeat element divergence in the K2P model distance to consensus is shown on the x-axis and the satDNA abundance on the y-axis. (a) TE exclusively observed in the genome of MSCU; (b-n) TEs shared between both species with more abundance in the MSCU genome; and (m-p) more abundance in the MQUA genome. (JPG 3167 KB)
Rights and permissions
About this article
Cite this article
Pereira, J.A., Milani, D., Ferretti, A.B.S.M. et al. The extensive amplification of heterochromatin in Melipona bees revealed by high throughput genomic and chromosomal analysis. Chromosoma 130, 251–262 (2021). https://doi.org/10.1007/s00412-021-00764-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-021-00764-x