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.

Learning retention mechanisms and evolutionary parameters of duplicate genes from their expression data

“…Therefore, to train CLOUD for both classification and prediction, we generated a balanced simulated dataset with 10 4 observations from each of the five classes, for a total of N = 50, 000 training observations. We assumed that tissues were independent, and that there were a total of m = 6 tissues as in an empirical data from Drosophila [Assis, 2019] that we later applied our method to, for a total of p = 108 input features.…”

“…Our simulation experiments highlight the exceptional classification performance of CLOUD relative to CDROM, as well as the unique ability of CLOUD to predict parameters underlying the evolution of duplicate genes. Hence, we next sought to use CLOUD to classify retention mechanisms and predict parameters of 208 duplicate genes in Drosophila [Assis and Bachtrog, 2013] from their expression data in six tissues [Assis, 2019]. Specifically, we first used PhyML [Guindon et al, 2010] to estimate a gene tree relating each parent, child, and ancestral gene in this dataset of duplicate genes [Assis and Bachtrog, 2013] (see Methods).…”

“…We applied CDROM and CLOUD to empirical data consisting of Drosophila duplicate and single-copy genes [Assis and Bachtrog, 2013] and their expression abundances in six tissues [Assis, 2019]. Because CLOUD requires estimates of T PC and T PCA , we first generated multiple sequence alignments with MACSE [Ranwez et al, 2018], which accounts for underlying codon structure, and then inferred a gene tree with PhyML [Guindon et al, 2010] for each parent, child, and ancestral gene in the duplication dataset [Assis and Bachtrog, 2013].…”

“…In previous work, Assis and Bachtrog [2013] tackled this problem by designing a decision tree classification algorithm based on comparisons of differences between multi-tissue expression profiles of ancestral singlecopy genes and their derived duplicate gene copies. This approach [Assis and Bachtrog, 2013], which was later generalized to other types of input data and implemented in the R package CDROM [Perry and Assis, 2016], has been used to classify retention mechanisms of duplicate genes in Drosophila [Assis and Bachtrog, 2013], mammals [Assis and Bachtrog, 2015], honeybees [Chau and Goodisman, 2017], and grasses [Jiang and Assis, 2019]. Together, these studies have demonstrated that duplicate genes are frequently retained by neofunctionalization [Assis and Bachtrog, 2013, Assis, 2014, Assis and Bachtrog, 2015, Chau and Goodisman, 2017, Jiang and Assis, 2019, that the young "child" copy more often acquires a new function than the original "parent" copy [Assis and Bachtrog, 2013, Assis, 2014, Assis and Bachtrog, 2015, Jiang and Assis, 2019, and that new functions tend to be male-specific [Assis and Bachtrog, 2013, Assis, 2014, Assis and Bachtrog, 2015, Chau and Goodisman, 2017, Jiang and Assis, 2019.…”

Transcription factors drive opposite relationships between gene age and tissue specificity in male and femaleDrosophilagonads

“…One clue is that older duplicated genes are more likely to be retained if they are ovary-biased (Assis, 2019). This might imply a specific importance of older genes to ovary expression and function.…”