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Unraveling the Genetic Basis for the Rapid Diversification of Male Genitalia between Drosophila Species

In the last 240,000 years, males of the Drosophila simulans species clade have evolved striking differences in the morphology of their epandrial posterior lobes and claspers (surstyli). These appendages are used for grasping the female during mating and so their divergence is most likely driven by s...

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Autores principales: Hagen, Joanna F D, Mendes, Cláudia C, Booth, Shamma R, Figueras Jimenez, Javier, Tanaka, Kentaro M, Franke, Franziska A, Baudouin-Gonzalez, Luis, Ridgway, Amber M, Arif, Saad, Nunes, Maria D S, McGregor, Alistair P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7826188/
https://www.ncbi.nlm.nih.gov/pubmed/32931587
http://dx.doi.org/10.1093/molbev/msaa232
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author Hagen, Joanna F D
Mendes, Cláudia C
Booth, Shamma R
Figueras Jimenez, Javier
Tanaka, Kentaro M
Franke, Franziska A
Baudouin-Gonzalez, Luis
Ridgway, Amber M
Arif, Saad
Nunes, Maria D S
McGregor, Alistair P
author_facet Hagen, Joanna F D
Mendes, Cláudia C
Booth, Shamma R
Figueras Jimenez, Javier
Tanaka, Kentaro M
Franke, Franziska A
Baudouin-Gonzalez, Luis
Ridgway, Amber M
Arif, Saad
Nunes, Maria D S
McGregor, Alistair P
author_sort Hagen, Joanna F D
collection PubMed
description In the last 240,000 years, males of the Drosophila simulans species clade have evolved striking differences in the morphology of their epandrial posterior lobes and claspers (surstyli). These appendages are used for grasping the female during mating and so their divergence is most likely driven by sexual selection. Mapping studies indicate a highly polygenic and generally additive genetic basis for these morphological differences. However, we have limited understanding of the gene regulatory networks that control the development of genital structures and how they evolved to result in this rapid phenotypic diversification. Here, we used new D. simulans/D. mauritiana introgression lines on chromosome arm 3L to generate higher resolution maps of posterior lobe and clasper differences between these species. We then carried out RNA-seq on the developing genitalia of both species to identify the expressed genes and those that are differentially expressed between the two species. This allowed us to test the function of expressed positional candidates during genital development in D. melanogaster. We identified several new genes involved in the development and possibly the evolution of these genital structures, including the transcription factors Hairy and Grunge. Furthermore, we discovered that during clasper development Hairy negatively regulates tartan (trn), a gene known to contribute to divergence in clasper morphology. Taken together, our results provide new insights into the regulation of genital development and how this has evolved between species.
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spelling pubmed-78261882021-01-27 Unraveling the Genetic Basis for the Rapid Diversification of Male Genitalia between Drosophila Species Hagen, Joanna F D Mendes, Cláudia C Booth, Shamma R Figueras Jimenez, Javier Tanaka, Kentaro M Franke, Franziska A Baudouin-Gonzalez, Luis Ridgway, Amber M Arif, Saad Nunes, Maria D S McGregor, Alistair P Mol Biol Evol Discoveries In the last 240,000 years, males of the Drosophila simulans species clade have evolved striking differences in the morphology of their epandrial posterior lobes and claspers (surstyli). These appendages are used for grasping the female during mating and so their divergence is most likely driven by sexual selection. Mapping studies indicate a highly polygenic and generally additive genetic basis for these morphological differences. However, we have limited understanding of the gene regulatory networks that control the development of genital structures and how they evolved to result in this rapid phenotypic diversification. Here, we used new D. simulans/D. mauritiana introgression lines on chromosome arm 3L to generate higher resolution maps of posterior lobe and clasper differences between these species. We then carried out RNA-seq on the developing genitalia of both species to identify the expressed genes and those that are differentially expressed between the two species. This allowed us to test the function of expressed positional candidates during genital development in D. melanogaster. We identified several new genes involved in the development and possibly the evolution of these genital structures, including the transcription factors Hairy and Grunge. Furthermore, we discovered that during clasper development Hairy negatively regulates tartan (trn), a gene known to contribute to divergence in clasper morphology. Taken together, our results provide new insights into the regulation of genital development and how this has evolved between species. Oxford University Press 2020-09-15 /pmc/articles/PMC7826188/ /pubmed/32931587 http://dx.doi.org/10.1093/molbev/msaa232 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
Hagen, Joanna F D
Mendes, Cláudia C
Booth, Shamma R
Figueras Jimenez, Javier
Tanaka, Kentaro M
Franke, Franziska A
Baudouin-Gonzalez, Luis
Ridgway, Amber M
Arif, Saad
Nunes, Maria D S
McGregor, Alistair P
Unraveling the Genetic Basis for the Rapid Diversification of Male Genitalia between Drosophila Species
title Unraveling the Genetic Basis for the Rapid Diversification of Male Genitalia between Drosophila Species
title_full Unraveling the Genetic Basis for the Rapid Diversification of Male Genitalia between Drosophila Species
title_fullStr Unraveling the Genetic Basis for the Rapid Diversification of Male Genitalia between Drosophila Species
title_full_unstemmed Unraveling the Genetic Basis for the Rapid Diversification of Male Genitalia between Drosophila Species
title_short Unraveling the Genetic Basis for the Rapid Diversification of Male Genitalia between Drosophila Species
title_sort unraveling the genetic basis for the rapid diversification of male genitalia between drosophila species
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7826188/
https://www.ncbi.nlm.nih.gov/pubmed/32931587
http://dx.doi.org/10.1093/molbev/msaa232
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