Out of the testis, into the ovary: biased outcomes of gene duplication and deletion in Drosophila

Raquel Assis

Research output: Contribution to journalArticle

Abstract

Gene turnover is a key source of adaptive variation. Yet most evolutionary studies have focused on gene duplication, dismissing gene deletion as a mechanism that simply eradicates redundancy. Here, I use genome-scale sequence and multi-tissue expression data from Drosophila melanogaster and Drosophila pseudoobscura to simultaneously assess the evolutionary outcomes of gene duplication and deletion in Drosophila. I find that gene duplication is more frequent than gene deletion in both species, indicating that it may play a more important role in Drosophila evolution. However, examination of several genic properties reveals that genes likely possess distinct functions after duplication that diverge further before deletion, suggesting that loss of redundancy cannot explain a majority of gene deletion events in Drosophila. Moreover, in addition to providing support for the well-known “out of the testis” origin of young duplicate genes, analyses of gene expression profiles uncover a preferential bias against deletion of old ovary-expressed genes. Therefore, I propose a novel “into the ovary” hypothesis for gene deletion in Drosophila, in which gene deletion may promote adaptation by salvaging genes that contribute to the evolution of female reproductive phenotypes. Under this combined “out of the testis, into the ovary” evolutionary model, gene duplication and deletion work in concert to generate and maintain a balanced repertoire of genes that promote sex-specific adaptation in Drosophila.

Original languageEnglish (US)
Pages (from-to)1850-1862
Number of pages13
JournalEvolution
Volume73
Issue number9
DOIs
StatePublished - Sep 1 2019

Fingerprint

Gene Duplication
gene deletion
Gene Deletion
gene duplication
Drosophila
Testis
Ovary
testes
gene
Genes
genes
Duplicate Genes
Drosophila pseudoobscura
duplicate genes
Drosophila melanogaster
Transcriptome
Genome
salvaging
Phenotype
phenotype

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Agricultural and Biological Sciences(all)

Cite this

@article{c4b6382fed694df2bea4acbdc60b20c6,
title = "Out of the testis, into the ovary: biased outcomes of gene duplication and deletion in Drosophila",
abstract = "Gene turnover is a key source of adaptive variation. Yet most evolutionary studies have focused on gene duplication, dismissing gene deletion as a mechanism that simply eradicates redundancy. Here, I use genome-scale sequence and multi-tissue expression data from Drosophila melanogaster and Drosophila pseudoobscura to simultaneously assess the evolutionary outcomes of gene duplication and deletion in Drosophila. I find that gene duplication is more frequent than gene deletion in both species, indicating that it may play a more important role in Drosophila evolution. However, examination of several genic properties reveals that genes likely possess distinct functions after duplication that diverge further before deletion, suggesting that loss of redundancy cannot explain a majority of gene deletion events in Drosophila. Moreover, in addition to providing support for the well-known “out of the testis” origin of young duplicate genes, analyses of gene expression profiles uncover a preferential bias against deletion of old ovary-expressed genes. Therefore, I propose a novel “into the ovary” hypothesis for gene deletion in Drosophila, in which gene deletion may promote adaptation by salvaging genes that contribute to the evolution of female reproductive phenotypes. Under this combined “out of the testis, into the ovary” evolutionary model, gene duplication and deletion work in concert to generate and maintain a balanced repertoire of genes that promote sex-specific adaptation in Drosophila.",
author = "Raquel Assis",
year = "2019",
month = "9",
day = "1",
doi = "10.1111/evo.13820",
language = "English (US)",
volume = "73",
pages = "1850--1862",
journal = "Evolution; international journal of organic evolution",
issn = "0014-3820",
publisher = "Society for the Study of Evolution",
number = "9",

}

Out of the testis, into the ovary : biased outcomes of gene duplication and deletion in Drosophila. / Assis, Raquel.

In: Evolution, Vol. 73, No. 9, 01.09.2019, p. 1850-1862.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Out of the testis, into the ovary

T2 - biased outcomes of gene duplication and deletion in Drosophila

AU - Assis, Raquel

PY - 2019/9/1

Y1 - 2019/9/1

N2 - Gene turnover is a key source of adaptive variation. Yet most evolutionary studies have focused on gene duplication, dismissing gene deletion as a mechanism that simply eradicates redundancy. Here, I use genome-scale sequence and multi-tissue expression data from Drosophila melanogaster and Drosophila pseudoobscura to simultaneously assess the evolutionary outcomes of gene duplication and deletion in Drosophila. I find that gene duplication is more frequent than gene deletion in both species, indicating that it may play a more important role in Drosophila evolution. However, examination of several genic properties reveals that genes likely possess distinct functions after duplication that diverge further before deletion, suggesting that loss of redundancy cannot explain a majority of gene deletion events in Drosophila. Moreover, in addition to providing support for the well-known “out of the testis” origin of young duplicate genes, analyses of gene expression profiles uncover a preferential bias against deletion of old ovary-expressed genes. Therefore, I propose a novel “into the ovary” hypothesis for gene deletion in Drosophila, in which gene deletion may promote adaptation by salvaging genes that contribute to the evolution of female reproductive phenotypes. Under this combined “out of the testis, into the ovary” evolutionary model, gene duplication and deletion work in concert to generate and maintain a balanced repertoire of genes that promote sex-specific adaptation in Drosophila.

AB - Gene turnover is a key source of adaptive variation. Yet most evolutionary studies have focused on gene duplication, dismissing gene deletion as a mechanism that simply eradicates redundancy. Here, I use genome-scale sequence and multi-tissue expression data from Drosophila melanogaster and Drosophila pseudoobscura to simultaneously assess the evolutionary outcomes of gene duplication and deletion in Drosophila. I find that gene duplication is more frequent than gene deletion in both species, indicating that it may play a more important role in Drosophila evolution. However, examination of several genic properties reveals that genes likely possess distinct functions after duplication that diverge further before deletion, suggesting that loss of redundancy cannot explain a majority of gene deletion events in Drosophila. Moreover, in addition to providing support for the well-known “out of the testis” origin of young duplicate genes, analyses of gene expression profiles uncover a preferential bias against deletion of old ovary-expressed genes. Therefore, I propose a novel “into the ovary” hypothesis for gene deletion in Drosophila, in which gene deletion may promote adaptation by salvaging genes that contribute to the evolution of female reproductive phenotypes. Under this combined “out of the testis, into the ovary” evolutionary model, gene duplication and deletion work in concert to generate and maintain a balanced repertoire of genes that promote sex-specific adaptation in Drosophila.

UR - http://www.scopus.com/inward/record.url?scp=85072057728&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85072057728&partnerID=8YFLogxK

U2 - 10.1111/evo.13820

DO - 10.1111/evo.13820

M3 - Article

C2 - 31418820

AN - SCOPUS:85072057728

VL - 73

SP - 1850

EP - 1862

JO - Evolution; international journal of organic evolution

JF - Evolution; international journal of organic evolution

SN - 0014-3820

IS - 9

ER -