The evolution of ovary-biased gene expression in Hawaiian Drosophila

Abstract

With detailed data on gene expression accessible from an increasingly broad array of species, we can test the extent to which our developmental genetic knowledge from model organisms predicts expression patterns and variation across species. But to know when differences in gene expression across species are significant, we first need to know how much evolutionary variation in gene expression we expect to observe. Here we provide an answer by analyzing RNAseq data across twelve species of Hawaiian Drosophilidae flies, focusing on gene expression differences between the ovary and other tissues. We show that over evolutionary time, there exists a cohort of ovary specific genes that is stable and that largely corresponds to described expression patterns from laboratory model Drosophila species. Our results also provide a demonstration of the prediction that, as phylogenetic distance increases, variation between species overwhelms variation between tissue types. Using ancestral state reconstruction of expression, we describe the distribution of evolutionary changes in tissue-biased expression, and use this to identify gains and losses of ovary-biased expression across these twelve species. We then use this distribution to calculate the evolutionary correlation in expression changes between genes, and demonstrate that genes with known interactions in D. melanogaster are significantly more correlated in their evolution than genes with no or unknown interactions. Finally, we use this correlation matrix to infer new networks of genes that share evolutionary trajectories, and we present these results as a dataset of new testable hypotheses about genetic roles and interactions in the function and evolution of the Drosophila ovary.

Integrating phylogenies into single-cell RNA sequencing analysis allows comparisons across species, genes, and cells

“…Shifting toward a phylogenetic approach to comparative scRNA-seq analysis unlocks new avenues of discovery, including tests of coevolution of cellular gene expression and other features of interest [9], as well as evolutionary screens for signatures of correlated gene and cell modules [19]. In phylogenetic analyses, statistical power depends on the number of independent evolutionary events rather than on the absolute number of taxa [8].…”

“…One option is to use summary statistics, such as the sum or average expression per species for genes within a homology group [26]. However, these statistics might obscure or average over real biological variation in expression that arose subsequent to a duplication event (among paralogs) [19]. An alternative approach is to connect genes via a similarity matrix, and then make all-by-all comparisons that are weighted on the basis of putative homology [7].…”

“…Other approaches (e.g., LIGER [37] or Seurat [38]) are reportedly able to distinguish and characterize species-specific differences [23]. Given that null hypotheses are still being developed [16] for how much variation in expression is expected to be observed across species [19], we hold that cross-species integration should be treated with caution until elucidation of the approach can robustly target and strictly remove technical batch effects.…”

Comparative Analysis of Maternal Gene Expression Patterns Unravels Evolutionary Signatures Across Reproductive Modes

“…Focus has been given to mammalian organ gene expression evolution ( Brawand et al 2011 ; Guschanski et al 2017 ; Cardoso-Moreira et al 2019 ; Fukushima and Pollock 2020 ). Some studies ventured into elucidating narrower evolutionary questions, such as siphonophore transcriptome evolution ( Munro et al 2022 ) or the ovary specific gene expression in Drosophiliids ( Church et al 2023 ). All these studies share in common the use of phylogenetic comparative methods, an approach proposed by Felsenstein in his seminal article ( Felsenstein 1985 ).…”

Comparative analysis of maternal gene expression patterns unravels evolutionary signatures across reproductive modes

“…Focus has been given to mammalian organ gene expression evolution (Brawand et al, 2011; Cardoso-Moreira et al, 2019; Fukushima & Pollock, 2020; Guschanski et al, 2017). Some studies ventured into elucidating narrower evolutionary questions, such as siphonophore transcriptome evolution (Munro et al, 2022) or the ovary specific gene expression in Drosophiliids (Church et al, 2023). All these studies share in common the use of phylogenetic comparative methods, an approach proposed by Felsenstein in his seminal article (Felsenstein, 1985).…”