Polymorphism and Divergence of Novel Gene Expression Patterns in Drosophila melanogaster

Abstract

Transcriptomes may evolve by multiple mechanisms, including the evolution of novel genes, the evolution of transcript abundance, and the evolution of cell, tissue, or organ expression patterns. Here we focus on the last of these mechanisms in an investigation of tissue and organ shifts in gene expression in Drosophila melanogaster. In contrast to most investigations of expression evolution, we seek to provide a framework for understanding the mechanisms of novel expression patterns on a short population genetic timescale. To do so we generated population samples of D. melanogaster transcriptomes from five tissues: accessory gland, testis, larval salivary gland, female head, and first instar larva. We combined these data with comparable data from two outgroups to characterize gains and losses of expression, both polymorphic and fixed, in D. melanogaster. We observed a large number of gain or loss of expression phenotypes, most of which were polymorphic within D. melanogaster. Several polymorphic, novel expression phenotypes were strongly influenced by segregating cis-acting variants. In support of previous literature on the evolution of novelties functioning in male reproduction, we observed many more novel expression phenotypes in the testis and accessory gland than in other tissues. Additionally, genes showing novel expression phenotypes tend to exhibit greater tissue specific expression. Finally, in addition to qualitatively novel expression phenotypes, we identified genes exhibiting major quantitative expression divergence in the D. melanogaster lineage.

Molecular Evolution across Mouse Spermatogenesis

“…There are many components or levels of molecular evolution, spanning from protein sequence changes to differences in gene expression level, timing, and developmental specificity (King and Wilson 1975;Betrán, et al 2002;Wray, et al 2003;Larracuente, et al 2008;Kaessmann 2010;Piasecka, et al 2013;Cridland, et al 2020). Many of these components have been shown to evolve relatively rapidly during spermatogenesis Khaitovich, et al 2005;Voolstra, et al 2007;Brawand, et al 2011;Kousathanas, et al 2014;Harrison, et al 2015;Vicens, et al 2017;Cridland, et al 2020;Sánchez-Ramírez, et al 2021), and generally trend towards increased divergence during the later stages of development (Good and Nachman 2005;Piasecka, et al 2013;Larson, et al 2016).…”

“…There are many components or levels of molecular evolution, spanning from protein sequence changes to differences in gene expression level, timing, and developmental specificity (King and Wilson 1975;Betrán, et al 2002;Wray, et al 2003;Larracuente, et al 2008;Kaessmann 2010;Piasecka, et al 2013;Cridland, et al 2020). Many of these components have been shown to evolve relatively rapidly during spermatogenesis Khaitovich, et al 2005;Voolstra, et al 2007;Brawand, et al 2011;Kousathanas, et al 2014;Harrison, et al 2015;Vicens, et al 2017;Cridland, et al 2020;Sánchez-Ramírez, et al 2021), and generally trend towards increased divergence during the later stages of development (Good and Nachman 2005;Piasecka, et al 2013;Larson, et al 2016). Novel genes disproportionately arise with testisspecific expression (Betrán, et al 2002;Levine, et al 2006;Kaessmann 2010;Assis and Bachtrog 2013;Zhao, et al 2014;Schroeder, et al 2019;Cridland, et al 2020;Lange, et al 2021), likely as a consequence of the more permissive regulatory environment of the later stages of sperm development (Kaessmann 2010;Soumillon, et al 2013).…”

“…Many of these components have been shown to evolve relatively rapidly during spermatogenesis Khaitovich, et al 2005;Voolstra, et al 2007;Brawand, et al 2011;Kousathanas, et al 2014;Harrison, et al 2015;Vicens, et al 2017;Cridland, et al 2020;Sánchez-Ramírez, et al 2021), and generally trend towards increased divergence during the later stages of development (Good and Nachman 2005;Piasecka, et al 2013;Larson, et al 2016). Novel genes disproportionately arise with testisspecific expression (Betrán, et al 2002;Levine, et al 2006;Kaessmann 2010;Assis and Bachtrog 2013;Zhao, et al 2014;Schroeder, et al 2019;Cridland, et al 2020;Lange, et al 2021), likely as a consequence of the more permissive regulatory environment of the later stages of sperm development (Kaessmann 2010;Soumillon, et al 2013). Likewise, the later stages of spermatogenesis tend to be enriched for novel testis-specific genes (Eddy 2002;Chalmel, et al 2007;Green, et al 2018).…”

“…These stage-specific patterns highlight the importance of studying specific components of molecular evolution in a developmental framework (Figure 1A; Larson, et al 2018a;Cutter and Bundus 2020). However, studies of molecular evolution have primarily focused on pairwise contrasts across nuanced aspects of tissue development (Good and Nachman 2005;Larson, et al 2016), or examined protein-coding versus regulatory evolution in whole tissues (Khaitovich, et al 2005;Voolstra, et al 2007;Larson, et al 2016;Mack, et al 2016;Vicens, et al 2017;Cridland, et al 2020), without combining both in a phylogenetic framework. Relying on whole tissue expression comparisons may be particularly problematic for spermatogenesis, because differences in testis composition are expected to evolve rapidly between species (Ramm and Schärer 2014;Yapar, et al 2021) and may confound patterns of expression level divergence (Good, et al 2010;Larson, et al 2016;Hunnicutt, et al 2021).…”

Single-nucleus transcriptomes reveal functional and evolutionary properties of cell types in the Drosophila accessory gland

“…Meiosis regulator and mRNA stability factor 1 ( Marf1 ) has low expression in sim and yak , but high expression and MC bias in mel (Fig 4 B ). Our previous work using bulk-tissue RNA-Seq described Marf1 as gaining “neomorphic” expression in the mel AG (Cridland et al 2020). Odorant-binding protein 58b ( Obp58b ) is highly expressed in sim , expressed moderately in yak , and rather lowly expressed in mel (Fig 4 B ).…”