Cargando…

Evolutionary Dynamics of Male Reproductive Genes in the Drosophila virilis Subgroup

Postcopulatory sexual selection (PCSS) is a potent evolutionary force that can drive rapid changes of reproductive genes within species, and thus has the potential to generate reproductive incompatibilities between species. Male seminal fluid proteins (SFPs) are major players in postmating interacti...

Descripción completa

Detalles Bibliográficos
Autores principales: Ahmed-Braimah, Yasir H., Unckless, Robert L., Clark, Andrew G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Genetics Society of America 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5592939/
https://www.ncbi.nlm.nih.gov/pubmed/28739599
http://dx.doi.org/10.1534/g3.117.1136
_version_ 1783262965017870336
author Ahmed-Braimah, Yasir H.
Unckless, Robert L.
Clark, Andrew G.
author_facet Ahmed-Braimah, Yasir H.
Unckless, Robert L.
Clark, Andrew G.
author_sort Ahmed-Braimah, Yasir H.
collection PubMed
description Postcopulatory sexual selection (PCSS) is a potent evolutionary force that can drive rapid changes of reproductive genes within species, and thus has the potential to generate reproductive incompatibilities between species. Male seminal fluid proteins (SFPs) are major players in postmating interactions, and are important targets of PCSS in males. The virilis subgroup of Drosophila exhibits strong interspecific gametic incompatibilities, and can serve as a model to study the genetic basis of PCSS and gametic isolation. However, reproductive genes in this group have not been characterized. Here we utilize short-read RNA sequencing of male reproductive organs to examine the evolutionary dynamics of reproductive genes in members of the virilis subgroup: D. americana, D. lummei, D. novamexicana, and D. virilis. We find that the majority of male reproductive transcripts are testes-biased, accounting for ∼15% of all annotated genes. Ejaculatory bulb (EB)-biased transcripts largely code for lipid metabolic enzymes, and contain orthologs of the D. melanogaster EB protein, Peb-me, which is involved in mating-plug formation. In addition, we identify 71 candidate SFPs, and show that this gene set has the highest rate of nonsynonymous codon substitution relative to testes- and EB-biased genes. Furthermore, we identify orthologs of 35 D. melanogaster SFPs that have conserved accessory gland expression in the virilis group. Finally, we show that several of the SFPs that have the highest rate of nonsynonymous codon substitution reside on chromosomal regions, which contributes to paternal gametic incompatibility between species. Our results show that SFPs rapidly diversify in the virilis group, and suggest that they likely play a role in PCSS and/or gametic isolation.
format Online
Article
Text
id pubmed-5592939
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher Genetics Society of America
record_format MEDLINE/PubMed
spelling pubmed-55929392017-09-14 Evolutionary Dynamics of Male Reproductive Genes in the Drosophila virilis Subgroup Ahmed-Braimah, Yasir H. Unckless, Robert L. Clark, Andrew G. G3 (Bethesda) Investigations Postcopulatory sexual selection (PCSS) is a potent evolutionary force that can drive rapid changes of reproductive genes within species, and thus has the potential to generate reproductive incompatibilities between species. Male seminal fluid proteins (SFPs) are major players in postmating interactions, and are important targets of PCSS in males. The virilis subgroup of Drosophila exhibits strong interspecific gametic incompatibilities, and can serve as a model to study the genetic basis of PCSS and gametic isolation. However, reproductive genes in this group have not been characterized. Here we utilize short-read RNA sequencing of male reproductive organs to examine the evolutionary dynamics of reproductive genes in members of the virilis subgroup: D. americana, D. lummei, D. novamexicana, and D. virilis. We find that the majority of male reproductive transcripts are testes-biased, accounting for ∼15% of all annotated genes. Ejaculatory bulb (EB)-biased transcripts largely code for lipid metabolic enzymes, and contain orthologs of the D. melanogaster EB protein, Peb-me, which is involved in mating-plug formation. In addition, we identify 71 candidate SFPs, and show that this gene set has the highest rate of nonsynonymous codon substitution relative to testes- and EB-biased genes. Furthermore, we identify orthologs of 35 D. melanogaster SFPs that have conserved accessory gland expression in the virilis group. Finally, we show that several of the SFPs that have the highest rate of nonsynonymous codon substitution reside on chromosomal regions, which contributes to paternal gametic incompatibility between species. Our results show that SFPs rapidly diversify in the virilis group, and suggest that they likely play a role in PCSS and/or gametic isolation. Genetics Society of America 2017-07-26 /pmc/articles/PMC5592939/ /pubmed/28739599 http://dx.doi.org/10.1534/g3.117.1136 Text en Copyright © 2017 Ahmed-Braimah et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Investigations
Ahmed-Braimah, Yasir H.
Unckless, Robert L.
Clark, Andrew G.
Evolutionary Dynamics of Male Reproductive Genes in the Drosophila virilis Subgroup
title Evolutionary Dynamics of Male Reproductive Genes in the Drosophila virilis Subgroup
title_full Evolutionary Dynamics of Male Reproductive Genes in the Drosophila virilis Subgroup
title_fullStr Evolutionary Dynamics of Male Reproductive Genes in the Drosophila virilis Subgroup
title_full_unstemmed Evolutionary Dynamics of Male Reproductive Genes in the Drosophila virilis Subgroup
title_short Evolutionary Dynamics of Male Reproductive Genes in the Drosophila virilis Subgroup
title_sort evolutionary dynamics of male reproductive genes in the drosophila virilis subgroup
topic Investigations
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5592939/
https://www.ncbi.nlm.nih.gov/pubmed/28739599
http://dx.doi.org/10.1534/g3.117.1136
work_keys_str_mv AT ahmedbraimahyasirh evolutionarydynamicsofmalereproductivegenesinthedrosophilavirilissubgroup
AT uncklessrobertl evolutionarydynamicsofmalereproductivegenesinthedrosophilavirilissubgroup
AT clarkandrewg evolutionarydynamicsofmalereproductivegenesinthedrosophilavirilissubgroup