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A long non-coding RNA is a key factor in the evolution of insect eusociality

View ORCID ProfileCarlos A. M. Cardoso-Junior, Gustavo J. Tibério, View ORCID ProfileDenyse C. Lago, Luiz Carlos Vieira, José C. Rosa, View ORCID ProfileAlexandre R. Paschoal, View ORCID ProfileIsobel Ronai, View ORCID ProfileBenjamin P. Oldroyd, View ORCID ProfileKlaus Hartfelder
doi: https://doi.org/10.1101/2022.05.10.491402
Carlos A. M. Cardoso-Junior
1Departamento de Biologia Celular e Molecular, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil.
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Gustavo J. Tibério
1Departamento de Biologia Celular e Molecular, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil.
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Denyse C. Lago
2Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil.
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Luiz Carlos Vieira
1Departamento de Biologia Celular e Molecular, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil.
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José C. Rosa
1Departamento de Biologia Celular e Molecular, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil.
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Alexandre R. Paschoal
3Universidade Tecnológica Federal do Paraná, Cornélio Procópio, PR, Brazil.
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Isobel Ronai
4Behaviour, Ecology and Evolution (BEE) laboratory, Macleay Building A12, University of Sydney, Sydney NSW 2006, Australia.
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Benjamin P. Oldroyd
4Behaviour, Ecology and Evolution (BEE) laboratory, Macleay Building A12, University of Sydney, Sydney NSW 2006, Australia.
5Wissenschaftskolleg zu Berlin, Wallotstrasse 19 D-14193, Berlin, Germany.
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Klaus Hartfelder
1Departamento de Biologia Celular e Molecular, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil.
2Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil.
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  • For correspondence: klaus@fmrp.usp.br
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SUMMARY

Insect sociality is a major evolutionary transition based on the suppression of worker reproduction in favor of the reproductive monopoly of the queen. In the honey bee (Apis mellifera) model organism, the development of the two female caste phenotypes, queen and worker, is triggered by differences in their larval diets. However, the mechanistic details underlying their respective developmental trajectories, as well as the maintenance of sterility in the adult workers, are still not fully understood. Here we show that the long non-coding RNA lncov1 interacts with the Tudor staphylococcus nuclease (Tudor-SN) protein to form a regulatory module that promotes apoptosis in the ovaries of worker larvae. In adult workers, the lncov1/Tudor-SN module responds positively to environmental cues that suppress reproductive capacity. As lncov1 is considerably conserved in the Apidae, we propose that, by promoting worker sterility, the lncov1/Tudor-SN module has likely played critical roles in the social evolution of bees.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵6 Lead contact.

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Posted May 11, 2022.
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A long non-coding RNA is a key factor in the evolution of insect eusociality
Carlos A. M. Cardoso-Junior, Gustavo J. Tibério, Denyse C. Lago, Luiz Carlos Vieira, José C. Rosa, Alexandre R. Paschoal, Isobel Ronai, Benjamin P. Oldroyd, Klaus Hartfelder
bioRxiv 2022.05.10.491402; doi: https://doi.org/10.1101/2022.05.10.491402
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A long non-coding RNA is a key factor in the evolution of insect eusociality
Carlos A. M. Cardoso-Junior, Gustavo J. Tibério, Denyse C. Lago, Luiz Carlos Vieira, José C. Rosa, Alexandre R. Paschoal, Isobel Ronai, Benjamin P. Oldroyd, Klaus Hartfelder
bioRxiv 2022.05.10.491402; doi: https://doi.org/10.1101/2022.05.10.491402

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