Intronization Signatures in Coding Exons Reveal the Evolutionary Fluidity of Eukaryotic Gene Architecture.

The conventionally clear distinction between exons and introns in eukaryotic genes is actually blurred. To illustrate this point, consider sequences that are retained in mature mRNAs about 50% of the time: how should they be classified? Moreover, although it is clear that RNA splicing influences gene expression levels and is an integral part of interdependent cellular networks, introns continue to be regarded as accidental insertions; exogenous sequences whose evolutionary origin is independent of mRNA-associated processes and somewhat still elusive. Here, we present evidence that aids to resolve this disconnect between conventional views about introns and current knowledge about the role of RNA splicing in the eukaryotic cell. We first show that coding sequences flanked by cryptic splice sites are negatively selected on a genome-wide scale in Paramecium. Then, we exploit selection intensity to infer splicing-related evolutionary dynamics. Our analyses suggest that intron gain begins as a splicing error, involves a transient phase of alternative splicing, and is preferentially completed at the 5' end of genes, which through intron gain can become highly expressed. We conclude that relaxed selective constraints may promote biological complexity in Paramecium and that the relationship between exons and introns is fluid on an evolutionary scale.

Gene Coexpression Network Reveals Highly Conserved, Well-Regulated Anti-Ageing Mechanisms in Old Ant Queens.

Evolutionary theories of ageing predict a reduction in selection efficiency with age, a so-called "selection shadow," due to extrinsic mortality decreasing effective population size with age. Classic symptoms of ageing include a deterioration in transcriptional regulation and protein homeostasis. Understanding how ant queens defy the trade-off between fecundity and lifespan remains a major challenge for the evolutionary theory of ageing. It has often been discussed that the low extrinsic mortality of ant queens, that are generally well protected within the nest by workers and soldiers, should reduce the selection shadow acting on old queens. We tested this by comparing strength of selection acting on genes upregulated in young and old queens of the ant, Cardiocondyla obscurior. In support of a reduced selection shadow, we find old-biased genes to be under strong purifying selection. We also analyzed a gene coexpression network (GCN) with the aim to detect signs of ageing in the form of deteriorating regulation and proteostasis. We find no evidence for ageing. In fact, we detect higher connectivity in old queens indicating increased transcriptional regulation with age. Within the GCN, we discover five highly correlated modules that are upregulated with age. These old-biased modules regulate several antiageing mechanisms such as maintenance of proteostasis, transcriptional regulation, and stress response. We observe stronger purifying selection on central hub genes of these old-biased modules compared with young-biased modules. These results indicate a lack of transcriptional ageing in old C. obscurior queens, possibly facilitated by strong selection at old age and well-regulated antiageing mechanisms.