The evolution of gene expression levels in mammalian organs

Abstract

Changes in gene expression are thought to underlie many of the phenotypic differences between species. However, large-scale analyses of gene expression evolution were until recently prevented by technological limitations. Here we report the sequencing of polyadenylated RNA from six organs across ten species that represent all major mammalian lineages (placentals, marsupials and monotremes) and birds (the evolutionary outgroup), with the goal of understanding the dynamics of mammalian transcriptome evolution. We show that the rate of gene expression evolution varies among organs, lineages and chromosomes, owing to differences in selective pressures: transcriptome change was slow in nervous tissues and rapid in testes, slower in rodents than in apes and monotremes, and rapid for the X chromosome right after its formation. Although gene expression evolution in mammals was strongly shaped by purifying selection, we identify numerous potentially selectively driven expression switches, which occurred at different rates across lineages and tissues and which probably contributed to the specific organ biology of various mammals.

Comparative transcriptomics across 14 Drosophila species reveals signatures of longevity

“…the vertical axis of Figure 2c). For comparison, a similar analysis was performed using the brain and liver data of nine mammalian species (Brawand et al., 2011), but the plateau feature was not as strong (Figure S3b,c). Since Drosophila diverged more recently than the mammals, it was surprising to see the plateau feature in the former but not the later.…”

“…To determine whether the evolutionary relationship of these species was reflected in their expression variation, we constructed gene expression phylograms using a distance matrix of 1 minus Spearman correlation coefficients and the neighbor‐joining method (Brawand et al., 2011; Clark et al., 2007). The resulting topology was largely consistent with their phylogeny (Figure 2a).…”

“…In the absence of selective pressure, the variation between a pair of species is expected to increase linearly with divergence time and can be modeled by a Brownian motion (BM) process (Felsenstein, 1985); this has been observed for transcription of many genes in mammals (especially among primates; Brawand et al., 2011; Khaitovich et al., 2004). On the other hand, previous studies based on genomes and transcriptomes observed that a large fraction of the genes in Drosophila were likely subjected to stabilizing selection (Bedford & Hartl, 2009; Clark et al., 2007; Kalinka et al., 2010; Rifkin, Kim & White, 2003), such that the increase in gene expression divergence eventually reaches a plateau (Bedford & Hartl, 2009) and may be better described by Ornstein‐Uhlenbeck (OU) process (Butler & King, 2004; Martins & Hansen, 1997).…”

“…Reliability of the branching pattern was assessed by a 1,000‐time bootstrap across the genes, using “boot.phylo” function of R package “ape” and random sampling of the expression set with replacement. For the mammalian dataset (Brawand et al., 2011), the amino acid sequence alignments of eight mammalian species (human, gorilla, chimpanzee, orangutan, macaque, mouse, opossum, and platypus) were extracted from the 46‐way multiple alignment in UCSC genome browser (Kuhn, Haussler & Kent, 2013). The species divergence time was based on TimeTree database (Hedges, Dudley & Kumar, 2006).…”

Gene expression profiling during the embryo‐to‐larva transition in the giant red sea urchin Mesocentrotus franciscanus

“…However , thanks to the advances in next‐generation sequencing (NGS) technologies, the ability to sequence the entire transcriptome of a given tissue or life‐history stage in a matter of days is providing new opportunities to explore the complexity of developmental GRNs in other echinoderms (Delroisse, Ortega‐Martinez, Dupont, Mallefet, & Flammang, 2015; Dilly, Gaitán‐Espitia, & Hofmann, 2015; Dylus et al., 2016; Gildor, Malik, Sher, Avraham, & Ben‐Tabou de‐Leon, 2015; Tulin, Aguiar, Istrail, & Smith, 2013) and marine invertebrates (Jackson & Degnan, 2016; Layden, Rentzsch, & Röttinger, 2016). As changes in gene expression may underlie many of the phenotypic differences between species (Brawand et al., 2011), studying transcriptomic divergence of sympatric species may shed light upon the initial genetic targets of natural selection in speciation events (Filteau, Pavey, St‐Cyr, & Bernatchez, 2013). Under this context, here we examine the transcriptome structure and the expression of genes during the embryo‐to‐larva transition of the giant red sea urchin Mesocentrotus franciscanus (syn.…”