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Multiple loci linked to inversions are associated with eye size variation in species of the Drosophila virilis phylad

Micael Reis, Gordon Wiegleb, Julien Claude, Rodrigo Lata, Britta Horchler, Ngoc-Thuy Ha, Christian Reimer, Cristina P. Vieira, Jorge Vieira, View ORCID ProfileNico Posnien
doi: https://doi.org/10.1101/2020.03.24.005413
Micael Reis
1University of Goettingen, Department of Developmental Biology, Göttingen Center for Molecular Biosciences (GZMB), Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany
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Gordon Wiegleb
1University of Goettingen, Department of Developmental Biology, Göttingen Center for Molecular Biosciences (GZMB), Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany
2International Max Planck Research School for Genome Science, Am Fassberg 11, 37077 Göttingen, Germany
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Julien Claude
3Institut des Sciences de l’Evolution de Montpellier, CNRS/UM2/IRD, 2 Place Eugène Bataillon, cc64, 34095 Montpellier Cedex 5, France
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Rodrigo Lata
4Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Portugal
5Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto, Portugal
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Britta Horchler
1University of Goettingen, Department of Developmental Biology, Göttingen Center for Molecular Biosciences (GZMB), Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany
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Ngoc-Thuy Ha
6University of Goettingen, Animal Breeding and Genetics Group, Department of Animal Sciences, Albrecht-Thaer-Weg 3, 37075 Göttingen, Germany
7University of Goettingen, Center for Integrated Breeding Research, Albrecht-Thaer-Weg 3, 37075 Göttingen, Germany
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Christian Reimer
6University of Goettingen, Animal Breeding and Genetics Group, Department of Animal Sciences, Albrecht-Thaer-Weg 3, 37075 Göttingen, Germany
7University of Goettingen, Center for Integrated Breeding Research, Albrecht-Thaer-Weg 3, 37075 Göttingen, Germany
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Cristina P. Vieira
4Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Portugal
5Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto, Portugal
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Jorge Vieira
4Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Portugal
5Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto, Portugal
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Nico Posnien
1University of Goettingen, Department of Developmental Biology, Göttingen Center for Molecular Biosciences (GZMB), Justus-von-Liebig-Weg 11, 37077 Göttingen, Germany
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  • ORCID record for Nico Posnien
  • For correspondence: nposnie@gwdg.de
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Abstract

The size and shape of organs is tightly controlled to achieve optimal function. Natural morphological variations often represent functional adaptations to an ever-changing environment. For instance, variation in head morphology is pervasive in insects and the underlying molecular basis is starting to be revealed in the Drosophila genus for species of the melanogaster group. However, it remains unclear whether similar diversifications are governed by similar or different molecular mechanisms over longer timescales. To address this issue, we used species of the virilis phylad because they have been diverging from D. melanogaster for at least 40 million years. Our comprehensive morphological survey revealed remarkable differences in eye size and head shape among these species with D. novamexicana having the smallest eyes and southern D. americana populations having the largest eyes. We show that the genetic architecture underlying eye size variation is complex with multiple associated genetic variants located on most chromosomes. Our genome wide association study (GWAS) strongly suggests that some of the putative causative variants are associated with the presence of inversions. Indeed, northern populations of D. americana share derived inversions with D. novamexicana and they show smaller eyes compared to southern ones. Intriguingly, we observed a significant enrichment of genes involved in eye development on the 4th chromosome after intersecting chromosomal regions associated with phenotypic differences with those showing high differentiation among D. americana populations. We propose that variants associated with chromosomal inversions contribute to both intra- and inter-specific variation in eye size among species of the virilis phylad.

Footnotes

  • MR: mreis{at}gwdg.de, GW: gordon.wiegleb{at}uni-goettingen.de, JC: julien.claude{at}umontpellier.fr, RL: rodrigoslata{at}gmail.com, BH: bkhorchler{at}web.de, NTH: nha{at}gwdg.de, CR: christian.reimer{at}agr.uni-goettingen.de, CPV: cgvieira{at}ibmc.up.pt, JV: jbvieira{at}ibmc.up.pt, NP: nposnie{at}gwdg.de

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Posted March 25, 2020.
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Multiple loci linked to inversions are associated with eye size variation in species of the Drosophila virilis phylad
Micael Reis, Gordon Wiegleb, Julien Claude, Rodrigo Lata, Britta Horchler, Ngoc-Thuy Ha, Christian Reimer, Cristina P. Vieira, Jorge Vieira, Nico Posnien
bioRxiv 2020.03.24.005413; doi: https://doi.org/10.1101/2020.03.24.005413
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Multiple loci linked to inversions are associated with eye size variation in species of the Drosophila virilis phylad
Micael Reis, Gordon Wiegleb, Julien Claude, Rodrigo Lata, Britta Horchler, Ngoc-Thuy Ha, Christian Reimer, Cristina P. Vieira, Jorge Vieira, Nico Posnien
bioRxiv 2020.03.24.005413; doi: https://doi.org/10.1101/2020.03.24.005413

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