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The extensive amplification of heterochromatin in Melipona bees revealed by high throughput genomic and chromosomal analysis

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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.

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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.

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Correspondence to Diogo C. Cabral-de-Mello or Denilce M. Lopes.

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Supplementary Information

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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)

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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

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