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Differences in orthodenticle expression promote ommatidial size variation between Drosophila species

View ORCID ProfileMontserrat Torres-Oliva, Elisa Buchberger, Alexandra D. Buffry, View ORCID ProfileMaike Kittelmann, View ORCID ProfileLauren Sumner-Rooney, Pedro Gaspar, Georg C. Bullinger, Genoveva Guerrero, View ORCID ProfileFernando Casares, View ORCID ProfileSaad Arif, View ORCID ProfileNico Posnien, View ORCID ProfileMaria D. S. Nunes, View ORCID ProfileAlistair P. McGregor, View ORCID ProfileIsabel Almudi
doi: https://doi.org/10.1101/2021.03.17.435774
Montserrat Torres-Oliva
1University Göttingen, Department of Developmental Biology, Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany
2Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, University Hospital Schleswig-Holstein, Kiel, Germany
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Elisa Buchberger
1University Göttingen, Department of Developmental Biology, Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany
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Alexandra D. Buffry
3Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, OX3 0BP, UK
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Maike Kittelmann
3Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, OX3 0BP, UK
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Lauren Sumner-Rooney
4Oxford University Museum of Natural History, Parks Road, Oxford OX1 3PW, UK
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Pedro Gaspar
3Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, OX3 0BP, UK
5MRC London Institute of Medical Sciences, London W12 0NN, UK
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Georg C. Bullinger
1University Göttingen, Department of Developmental Biology, Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany
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Genoveva Guerrero
6GEM-DMC2 Unit, CABD (CSIC-UPO-JA), Ctra. de Utrera km 1, 41013 Seville, Spain
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Fernando Casares
6GEM-DMC2 Unit, CABD (CSIC-UPO-JA), Ctra. de Utrera km 1, 41013 Seville, Spain
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Saad Arif
3Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, OX3 0BP, UK
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  • For correspondence: isabelalmudi@gmail.com
Nico Posnien
1University Göttingen, Department of Developmental Biology, Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany
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  • For correspondence: isabelalmudi@gmail.com
Maria D. S. Nunes
3Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, OX3 0BP, UK
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Alistair P. McGregor
3Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, OX3 0BP, UK
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Isabel Almudi
3Department of Biological and Medical Sciences, Oxford Brookes University, Oxford, OX3 0BP, UK
6GEM-DMC2 Unit, CABD (CSIC-UPO-JA), Ctra. de Utrera km 1, 41013 Seville, Spain
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  • For correspondence: isabelalmudi@gmail.com
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Abstract

The compound eyes of insects exhibit extensive variation in ommatidia number and size, which affects how they see and underlies adaptations in their vision to different environments and lifestyles. However, very little is known about the genetic and developmental bases underlying differences in compound eye size. We previously showed that the larger eyes of Drosophila mauritiana compared to D. simulans is caused by differences in ommatidia size rather than number. Furthermore, we identified an X-linked chromosomal region in D. mauritiana that results in larger eyes when introgressed into D. simulans. Here, we used a combination of fine-scale mapping and gene expression analysis to further investigate positional candidate genes on the X chromosome. We found that orthodenticle is expressed earlier in D. mauritiana than in D. simulans during ommatidial maturation in third instar larvae, and we further show that this gene is required for the correct organisation and size of ommatidia in D. melanogaster. Using ATAC-seq, we have identified several candidate eye enhancers of otd as well as potential direct targets of this transcription factor that are differentially expressed between D. mauritiana and D. simulans. Taken together, our results suggest that differential timing of otd expression contributes to natural variation in ommatidia size between D. mauritiana and D. simulans, which provides new insights into the mechanisms underlying the regulation and evolution of compound eye size in insects.

Competing Interest Statement

The authors have declared no competing interest.

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Differences in orthodenticle expression promote ommatidial size variation between Drosophila species
Montserrat Torres-Oliva, Elisa Buchberger, Alexandra D. Buffry, Maike Kittelmann, Lauren Sumner-Rooney, Pedro Gaspar, Georg C. Bullinger, Genoveva Guerrero, Fernando Casares, Saad Arif, Nico Posnien, Maria D. S. Nunes, Alistair P. McGregor, Isabel Almudi
bioRxiv 2021.03.17.435774; doi: https://doi.org/10.1101/2021.03.17.435774
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Differences in orthodenticle expression promote ommatidial size variation between Drosophila species
Montserrat Torres-Oliva, Elisa Buchberger, Alexandra D. Buffry, Maike Kittelmann, Lauren Sumner-Rooney, Pedro Gaspar, Georg C. Bullinger, Genoveva Guerrero, Fernando Casares, Saad Arif, Nico Posnien, Maria D. S. Nunes, Alistair P. McGregor, Isabel Almudi
bioRxiv 2021.03.17.435774; doi: https://doi.org/10.1101/2021.03.17.435774

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