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Variation in Pleiotropic Hub Gene Expression Is Associated with Interspecific Differences in Head Shape and Eye Size in Drosophila

Revealing the mechanisms underlying the breathtaking morphological diversity observed in nature is a major challenge in Biology. It has been established that recurrent mutations in hotspot genes cause the repeated evolution of morphological traits, such as body pigmentation or the gain and loss of s...

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Autores principales: Buchberger, Elisa, Bilen, Anıl, Ayaz, Sanem, Salamanca, David, Matas de las Heras, Cristina, Niksic, Armin, Almudi, Isabel, Torres-Oliva, Montserrat, Casares, Fernando, Posnien, Nico
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8097299/
https://www.ncbi.nlm.nih.gov/pubmed/33386848
http://dx.doi.org/10.1093/molbev/msaa335
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author Buchberger, Elisa
Bilen, Anıl
Ayaz, Sanem
Salamanca, David
Matas de las Heras, Cristina
Niksic, Armin
Almudi, Isabel
Torres-Oliva, Montserrat
Casares, Fernando
Posnien, Nico
author_facet Buchberger, Elisa
Bilen, Anıl
Ayaz, Sanem
Salamanca, David
Matas de las Heras, Cristina
Niksic, Armin
Almudi, Isabel
Torres-Oliva, Montserrat
Casares, Fernando
Posnien, Nico
author_sort Buchberger, Elisa
collection PubMed
description Revealing the mechanisms underlying the breathtaking morphological diversity observed in nature is a major challenge in Biology. It has been established that recurrent mutations in hotspot genes cause the repeated evolution of morphological traits, such as body pigmentation or the gain and loss of structures. To date, however, it remains elusive whether hotspot genes contribute to natural variation in the size and shape of organs. As natural variation in head morphology is pervasive in Drosophila, we studied the molecular and developmental basis of differences in compound eye size and head shape in two closely related Drosophila species. We show differences in the progression of retinal differentiation between species and we applied comparative transcriptomics and chromatin accessibility data to identify the GATA transcription factor Pannier (Pnr) as central factor associated with these differences. Although the genetic manipulation of Pnr affected multiple aspects of dorsal head development, the effect of natural variation is restricted to a subset of the phenotypic space. We present data suggesting that this developmental constraint is caused by the coevolution of expression of pnr and its cofactor u-shaped (ush). We propose that natural variation in expression or function of highly connected developmental regulators with pleiotropic functions is a major driver for morphological evolution and we discuss implications on gene regulatory network evolution. In comparison to previous findings, our data strongly suggest that evolutionary hotspots are not the only contributors to the repeated evolution of eye size and head shape in Drosophila.
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spelling pubmed-80972992021-05-10 Variation in Pleiotropic Hub Gene Expression Is Associated with Interspecific Differences in Head Shape and Eye Size in Drosophila Buchberger, Elisa Bilen, Anıl Ayaz, Sanem Salamanca, David Matas de las Heras, Cristina Niksic, Armin Almudi, Isabel Torres-Oliva, Montserrat Casares, Fernando Posnien, Nico Mol Biol Evol Discoveries Revealing the mechanisms underlying the breathtaking morphological diversity observed in nature is a major challenge in Biology. It has been established that recurrent mutations in hotspot genes cause the repeated evolution of morphological traits, such as body pigmentation or the gain and loss of structures. To date, however, it remains elusive whether hotspot genes contribute to natural variation in the size and shape of organs. As natural variation in head morphology is pervasive in Drosophila, we studied the molecular and developmental basis of differences in compound eye size and head shape in two closely related Drosophila species. We show differences in the progression of retinal differentiation between species and we applied comparative transcriptomics and chromatin accessibility data to identify the GATA transcription factor Pannier (Pnr) as central factor associated with these differences. Although the genetic manipulation of Pnr affected multiple aspects of dorsal head development, the effect of natural variation is restricted to a subset of the phenotypic space. We present data suggesting that this developmental constraint is caused by the coevolution of expression of pnr and its cofactor u-shaped (ush). We propose that natural variation in expression or function of highly connected developmental regulators with pleiotropic functions is a major driver for morphological evolution and we discuss implications on gene regulatory network evolution. In comparison to previous findings, our data strongly suggest that evolutionary hotspots are not the only contributors to the repeated evolution of eye size and head shape in Drosophila. Oxford University Press 2021-01-02 /pmc/articles/PMC8097299/ /pubmed/33386848 http://dx.doi.org/10.1093/molbev/msaa335 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) ), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Buchberger, Elisa
Bilen, Anıl
Ayaz, Sanem
Salamanca, David
Matas de las Heras, Cristina
Niksic, Armin
Almudi, Isabel
Torres-Oliva, Montserrat
Casares, Fernando
Posnien, Nico
Variation in Pleiotropic Hub Gene Expression Is Associated with Interspecific Differences in Head Shape and Eye Size in Drosophila
title Variation in Pleiotropic Hub Gene Expression Is Associated with Interspecific Differences in Head Shape and Eye Size in Drosophila
title_full Variation in Pleiotropic Hub Gene Expression Is Associated with Interspecific Differences in Head Shape and Eye Size in Drosophila
title_fullStr Variation in Pleiotropic Hub Gene Expression Is Associated with Interspecific Differences in Head Shape and Eye Size in Drosophila
title_full_unstemmed Variation in Pleiotropic Hub Gene Expression Is Associated with Interspecific Differences in Head Shape and Eye Size in Drosophila
title_short Variation in Pleiotropic Hub Gene Expression Is Associated with Interspecific Differences in Head Shape and Eye Size in Drosophila
title_sort variation in pleiotropic hub gene expression is associated with interspecific differences in head shape and eye size in drosophila
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8097299/
https://www.ncbi.nlm.nih.gov/pubmed/33386848
http://dx.doi.org/10.1093/molbev/msaa335
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