Origins, evolution, and phenotypic impact of new genes

Abstract

Ever since the pre-molecular era, the birth of new genes with novel functions has been considered to be a major contributor to adaptive evolutionary innovation. Here, I review the origin and evolution of new genes and their functions in eukaryotes, an area of research that has made rapid progress in the past decade thanks to the genomics revolution. Indeed, recent work has provided initial whole-genome views of the different types of new genes for a large number of different organisms. The array of mechanisms underlying the origin of new genes is compelling, extending way beyond the traditionally well-studied source of gene duplication. Thus, it was shown that novel genes also regularly arose from messenger RNAs of ancestral genes, protein-coding genes metamorphosed into new RNA genes, genomic parasites were coopted as new genes, and that both protein and RNA genes were composed from scratch (i.e., from previously nonfunctional sequences). These mechanisms then also contributed to the formation of numerous novel chimeric gene structures. Detailed functional investigations uncovered different evolutionary pathways that led to the emergence of novel functions from these newly minted sequences and, with respect to animals, attributed a potentially important role to one specific tissue-the testis-in the process of gene birth. Remarkably, these studies also demonstrated that novel genes of the various types significantly impacted the evolution of cellular, physiological, morphological, behavioral, and reproductive phenotypic traits. Consequently, it is now firmly established that new genes have indeed been major contributors to the origin of adaptive evolutionary novelties.What is the nature of mutations underlying adaptive evolutionary innovations? In addition to subtle genetic modifications of preexisting ancestral genes that can lead to differences in their (protein or RNA) sequences or activities, new genes with novel functions may have significantly contributed to the evolution of lineage-or species-specific phenotypic traits. Consequently, the process of the ''birth'' and evolution of novel genes has attracted much attention from biologists in the past. Indeed, quite remarkably, considerations pertaining to the origin and functional fate of new genes trace back to a time when the molecular nature of genes had not yet been established. Based on cytological observations of chromosomal duplications, Haldane (1933) and Muller (1935) already hypothesized in the 1930s that new gene functions may emerge from refashioned copies of old genes, highlighting for the first time the potential importance of gene duplication for the process of new gene origination. The early notions that gene duplication provides a significant reservoir for the emergence of genes and hence phenotypic adaptation have now been globally confirmed (but also refined) based on numerous large-and smallscale molecular studies that were facilitated by the genomics revolution. New duplicate genes have been shown to be abundant in all eukaryotic genomes ...

Intronless and intron-containing type I IFN genes coexist in amphibian Xenopus tropicalis : Insights into the origin and evolution of type I IFNs in vertebrates

“…Retroposition is an important molecular mechanism for the generation of new genes and acquisition of new functions, playing essential roles in adaptive evolution of organisms (Kaessmann, 2010). By means of retroposition, intron-containing type I IFN genes in amphibians may have lost their introns, and may have been rearranged into new genomic regions on different chromosomes as observed in the present loci of intronless type I IFN genes in vertebrates.…”

Gene duplication, tissue-specific gene expression and sexual conflict in stalk-eyed flies (Diopsidae)

“…Many of these duplicates may have resulted from selection pressures associated with sperm competition rather than sexual conflict. The rate of testes-specific duplication may also be enhanced by certain properties of transcription within this tissue, such as open chromatic structure and elevated levels of the core transcriptional machinery [149]. Second, the analysis of the head duplicates indicates that tissues other than the testes may be a rich source of sexual conflict that is resolved through gene duplication.…”

The Persistent Contributions of RNA to Eukaryotic Gen(om)e Architecture and Cellular Function

“…Gene duplication as a means of generating novel genes has been realized for a long time (Haldane 1933;Muller 1935;Bridges 1936;Lewis 1951;Stephens 1951;Nei 1969). Gradual change from a duplicated gene, via those encoding isoforms, up to the acquisition of novel functions including subfunctionalization (Lynch and Force 2000) is now well documented (Roth et al 2007;Kaessmann 2010;Chen et al 2013). Gene amplification can occur via segmental duplication (Bailey and Eichler 2006) or retroposition (Brosius 1999a;Babushok et al 2007) with a lower "success rate" for the latter.…”