Common Pattern of Evolution of Gene Expression Level and Protein Sequence in Drosophila

Abstract

Sequence divergence scaled by variation within species has been used to infer the action of selection upon individual genes. Applying this approach to expression, we compared whole-genome whole-body RNA levels in 10 heterozygous Drosophila simulans genotypes and a pooled sample of 10 D. melanogaster lines using Affymetrix Genechip. For 972 genes expressed in D. melanogaster, the transcript level was below detection threshold in D. simulans, which may be explained either by sequence divergence between the primers on the chip and the mRNA transcripts or by down-regulation of these genes. Out of 6,707 genes that were expressed in both species, transcript level was significantly different between species for 534 genes (at P < 0.001). Genes whose expression is under stabilizing selection should exhibit reduced genetic variation within species and reduced divergence between species. Expression of genes under directional selection in D. simulans should be highly divergent from D. melanogaster, while showing low genetic variation in D. simulans. Finally, the genes with large variation within species but modest divergence between species are candidates for balancing selection. Rapidly diverging, low-polymorphism genes included those involved in reproduction (e.g., Mst 3Ba, 98Cb; Acps 26Aa, 63F; and sperm-specific dynein). Genes with high variation in transcript abundance within species included metallothionein and hairless, both hypothesized to be segregating in nature because of gene-by-environment interactions. Further, we compared expression divergence and DNA substitution rate in 195 genes. Synonymous substitution rate and expression divergences were uncorrelated, whereas there was a significant positive correlation between nonsynonymous substitution rate and expression divergence. We hypothesize that as a substantial fraction of nonsynonymous divergence has been shown to be adaptive, much of the observed expression divergence is likewise adaptive.

Applications of next generation sequencing in molecular ecology of non-model organisms

“…As an example of this, (Dassanayake et al, 2009) used transcriptome characterization of two species of mangrove to investigate convergent evolution of gene expression. Shared transcriptomic profiles between species may of course be a result of a common evolutionary origin or a joint distribution (Nuzhdin et al, 2004). However, in the case of the two mangrove species investigated by Dassanayake et al, this is not likely to explain the pattern seen.…”

Constraint and turnover in sex-biased gene expression in the genus Drosophila

“…2c). Extensive (20%) categorical changes in sex-bias class, especially for genes with male-biased expression, were previously reported between D. melanogaster and D. simulans 12,13 . We observed a categorical change in sex-biased expression in 12% of the orthologues between these two species, but the changes were dominated by low magnitude changes between modest sex-biased expression and non-sex-biased categories.…”

Evaluating the role of natural selection in the evolution of gene regulation

“…Genome-wide measurements have revealed high rates of genetic variation in gene expression (typically 410% of genes) in humans (Enard et al, 2002;Rockman and Wray, 2002;Bray et al, 2003;Lo et al, 2003;Whitney et al, 2003;Morley et al, 2004;Pastinen et al, 2004;Radich et al, 2004), mice (Cowles et al, 2002;Schadt et al, 2003;Shockley and Churchill, 2006), fish (Oleksiak et al, 2002(Oleksiak et al, , 2005, flies (Jin et al, 2001;Wayne and McIntyre, 2002;Meiklejohn et al, 2003;Rifkin et al, 2003;Nuzhdin et al, 2004;Ranz et al, 2004), yeast (Cavalieri et al, 2000;Brem et al, 2002;Townsend et al, 2003;Yvert et al, 2003;Fay et al, 2004), plants (Kirst et al, 2005;Vuylsteke et al, 2005;Lai et al, 2006) and bacteria (Le et al, 2005). Patterns of expression divergence have also been compared between sexes (Jin et al, 2001;Ranz et al, 2003;Gibson et al, 2004), across developmental stages (Rifkin et al, 2003), among tissue types (Enard et al, 2002;Whitehead and Crawford, 2005;Khaitovich et al, 2005a, b) and over different environments (Fay et al, 2004;Landry et al, 2006).…”

“…For expression patterns driven by positive selection, large differences between species are expected despite little variation within a species. Although this approach does not distinguish between neutral and selected changes, it provides an interesting list of candidate genes for further study Nuzhdin et al, 2004;Gilad et al, 2006a, b). For example, using this ranking system, Gilad et al (2006a, b) showed that a significant fraction of candidate genes identified in a comparison of primate species were transcription factors.…”