No excess of cis -regulatory variation associated with intra-specific selection in wild pearl millet ( Cenchrus americanus )

Abstract

Several studies suggest that cis-regulatory mutations are the favorite target of evolutionary changes, one reason being that cis-regulatory mutations might have fewer deleterious pleiotropic effects than protein-coding mutations. A review of the process also suggests that this bias towards adaptive cis-regulatory variation might be less pronounced at the intraspecific level compared with the interspecific level. In this study, we assessed the contribution of cis-regulatory variation to adaptation at the intraspecific level using populations of wild pearl millet (Cenchrus americanus ssp. monodii) sampled along an environmental gradient in Niger. From RNA sequencing of hybrids to assess allele-specific expression, we identified genes with cis-regulatory divergence between two parental accessions collected in contrasted environmental conditions. This revealed that ∼15% of transcribed genes showed cis-regulatory variation. Intersecting the gene set exhibiting cis-regulatory variation with the gene set identified as targets of selection revealed no excess of cis-acting mutations among the selected genes. We additionally found no excess of cis-regulatory variation among genes associated with adaptive traits. As our approach relied on methods identifying mainly genes submitted to strong selection pressure or with high phenotypic effect, the contribution of cis-regulatory changes to soft selection or polygenic adaptive traits remains to be tested. However our results favor the hypothesis that enrichment of adaptive cis-regulatory divergence builds up over time. For short evolutionary time-scales, cis-acting mutations are not predominantly involved in adaptive evolution associated with strong selective signal.

Evolutionary transcriptomics reveals the origins of olives and the genomic changes associated with their domestication

“…Third, mutations in cis ‐regulatory regions (CREs) played a major role in changing expression patterns. CREs are known to be major targets of evolutionary changes, due to their weaker deleterious pleiotropic effects compared with mutations in coding sequences (Stern and Orgogozo, ), as was exemplified in annual crops (Lemmon et al ., ; Wang et al ., ; but see Rhoné et al ., ). Yet, they were not captured by our transcriptomic data and, in case of rapid decay of linkage disequilibrium, signatures of selection could not extend up to the coding regions we sequenced.…”

Inferring the genetic architecture of expression variation from replicated high throughput allele-specific expression experiments

“…Many results have been reported for a wide range of individuals, populations, or species (Tirosh et al 2009;Wittkopp, Haerum, and Clark 2008;McManus et al 2010;). Such inferences have been applied to questions about compensation between cis and trans variation (Romero, Ruvinsky, and Gilad 2012;Mack, Campbell, and Nachman 2016), stabilizing selection for expression level (Hodgins-Davis, Rice, and Townsend 2015), and cis-effect in inter-specific/intra-specific expression variation (Metzger, Wittkopp, and Coolon 2017;Rhoné et al 2017) and all depend in a central way on accurate measurement of cis variation. However, naive statistical models (Robinson and Smyth 2007) and the tendency to misuse replication has limited the utility of allele-specific-expression inference.…”

“…The cis effect parameter (e cis ) for a gene is defined as the ratio of the expression from allele 1 and allele 2 Schaefke et al 2013). However, previous allele-specific expression studies using RNA-seq for cis-effect typically employed 1-3 hybrid replicates in binomial framework Schaefke et al 2013;Metzger, Wittkopp, and Coolon 2017;Rhoné et al 2017;Mack, Campbell, and Nachman 2016;McManus et al 2014;Bell et al 2013), which assumes that the read counts for each allele among replicates can be modeled as a Poisson random variable.…”

Effects of a male meiotic driver on male and female transcriptomes in the house mouse

“…In ovaries, liver and brain, most expression changes were associated with genes of the t haplotype itself. Both cis and trans changes are important in adaptive evolution, but it appears that trans changes feature more prominently in adaptation within species, whereas cis changes play a larger role in divergence between species [58][59][60]. This is interesting in the context of the t haplotype because it is thought to have evolved 1-3 Ma [61,62] and then recently introgressed into Mus musculus populations, either from an isolated M. musculus lineage [12] or from another species [63].…”