Genes are perpetually added to and deleted from genomes during evolution. Thus, it is important to understand how new genes are formed and evolve as critical components of the genetic systems determining the biological diversity of life. Two decades of effort have shed light on the process of new gene origination, and have contributed to an emerging comprehensive picture of how new genes are added to genomes, ranging from the mechanisms that generate new gene structures to the presence of new genes in different organisms to the rates and patterns of new gene origination and the roles of new genes in phenotypic evolution. We review each of these aspects of new gene evolution, summarizing the main evidence for the origination and importance of new genes in evolution. We highlight findings showing that new genes rapidly change existing genetic systems that govern various molecular, cellular and phenotypic functions.

Mutations that add, subtract, rearrange, or otherwise refashion genome structure often affect phenotypes, though the fragmented nature of most contemporary assemblies obscure them. To discover such mutations, we assembled the first new reference quality genome of Drosophila melanogaster since its initial sequencing. By comparing this genome to the existing D. melanogaster assembly, we create a structural variant map of unprecedented resolution, revealing extensive genetic variation that has remained hidden until now. Many of these variants constitute strong candidates underlying phenotypic variation, including tandem duplications and a transposable element insertion that dramatically amplifies the expression of detoxification genes associated with nicotine resistance. The abundance of important genetic variation that still evades discovery highlights how crucial high-quality references are to deciphering phenotypes.

Males and females have different fitness optima but share vast majority of their genomes, causing an inherent genetic conflict between the two sexes that must be resolved to achieve maximal population fitness. We show that two tandem duplicate genes found specifically in Drosophila melanogaster are sexually antagonistic, but rapidly evolved sex-specific functions and expression patterns that mitigate their antagonistic effects. We use copy-specific knockouts and rescue experiments to show that Apollo is essential for male fertility but detrimental to female fertility, in addition to its important role in development, while Artemis is essential for female fertility but detrimental to male fertility. Further analyses show that Apl and Art have essential roles in spermatogenesis and oogenesis. These duplicates formed ~200,000 years ago, underwent a strong selective sweep and lost most expression in the antagonized sex. These data provide direct evidence that gene duplication allowed rapid mitigation of sexual conflict to evolve essential gametogenesis functions.

eTOC blurb Westerman, VanKuren et al. show that butterfly wing color maps to a putative cis-regulatory element adjacent to two aristaless genes. The genes are differentially expressed between white and yellow wings and CRISPR knockout of aristaless1 causes white wings to develop yellow. Both colors have been shared among species via hybridization.

The mycoplasma-related endobacteria (MRE), representing a recently discovered lineage of Mollicutes, are widely distributed across arbuscular mycorrhizal fungi (AMF, Glomeromycota). AMF colonize roots of most terrestrial plants and improve plant mineral nutrient uptake in return for plant-assimilated carbon. The role of MRE in the biology of their fungal hosts is unknown. To start characterizing this association, we assessed partitioning of MRE genetic diversity within AMF individuals and across the AMF phylogeographic range. We further used molecular evolution patterns to make inferences about MRE codivergence with AMF, their lifestyle and antiquity of the Glomeromycota-MRE association. While we did not detect differentiation between MRE derived from different continents, high levels of diversity were apparent in MRE populations within AMF host individuals. MRE exhibited significant codiversification with AMF over ecological time and the absence of codivergence over evolutionary time. Moreover, genetic recombination was evident in MRE. These patterns indicate that, while MRE transmission is predominantly vertical, their complex intrahost populations are likely generated by horizontal transmission and recombination. Based on predictions of evolutionary theory, we interpreted these observations as a suggestion that MRE may be antagonists of AMF. Finally, we detected a marginally significant signature of codivergence of MRE with Glomeromycota and the Endogone lineage of Mucoromycotina, implying that the symbiosis between MRE and fungi may predate the divergence between these two groups of fungi.

Arbuscular mycorrhizal (AM) fungi in the phylum Glomeromycota colonize roots of the majority of land plants and assist them in the uptake of mineral nutrients in exchange for plant-assimilated carbon. In the absence of sexual reproductive structures and with asexual spore morphology conserved since the Ordovician, Glomeromycota may be one of the oldest eukaryotic lineages that rely predominantly on asexual reproduction for gene transmission. Clonal population structure detected in the majority of AM fungi examined to date supports this hypothesis. However, evidence of recombination found in few local populations suggests that genetic exchanges may be more common in these organisms than is currently recognized. To explore the significance of clonal expansion versus genetic recombination in the life history of modern Glomeromycota, we examined the global population of a cosmopolitan fungus Glomus etunicatum and made inferences about the population structure and the occurrence of recombination in the history of this species. We sampled eight loci from 84 isolates. We found that although the global population of G. etunicatum showed a pattern of significant differentiation, several haplotypes had a broad geographic distribution spanning multiple continents. Molecular variation among the sampled isolates indicated an overwhelmingly clonal population structure and suggested that clonal expansion plays an important role in the ecological success of modern Glomeromycota. In contrast, a pattern of homoplasy consistent with a history of recombination suggested that gene exchanges are not completely absent from the life history of these organisms, although they are likely to be very rare.

Recent studies have revealed key roles of noncoding RNAs in sex-related pathways, but little is known about the evolutionary forces acting on these noncoding RNAs. Profiling the transcriptome of Drosophila melanogaster with whole-genome tiling arrays found that 15% of male-biased transcribed fragments are intergenic noncoding RNAs (incRNAs), suggesting a potentially important role for incRNAs in sex-related biological processes. Statistical analysis revealed a paucity of malebiased incRNAs and coding genes on the X chromosome, suggesting that similar evolutionary forces could be affecting the genomic organization of both coding and noncoding genes. Expression profiling across germline and somatic tissues further suggested that both male meiotic sex chromosome inactivation (MSCI) and sexual antagonism could contribute to the chromosomal distribution of male-biased incRNAs. Comparative sequence analysis showed that the evolutionary age of male-biased incRNAs is a significant predictor of their chromosomal locations. In addition to identifying abundant sexbiased incRNAs in the fly genome, our work unveils a global picture of the complex interplay between noncoding RNAs and sexual chromosome evolution.

Arbuscular mycorrhizal fungi (phylum Glomeromycota) are among the oldest and most successful symbionts of land plants. With no evidence of sexual reproduction, their evolutionary success is inconsistent with the prediction that asexual taxa are vulnerable to extinction due to accumulation of deleterious mutations. To explore why Glomeromycota defy this prediction, we studied ribosomal RNA (rRNA) gene evolution in the Claroideoglomus lineage and estimated effective population size, Ne, in C. etunicatum. We found that rRNA genes of these fungi exhibit unusual and complex patterns of molecular evolution. In C. etunicatum, these patterns can be collectively explained by an unexpectedly large Ne combined with imperfect genome‐wide and population‐level rRNA gene repeat homogenization. The mutations accumulated in rRNA gene sequences indicate that natural selection is effective at purging deleterious mutations in the Claroideoglomus lineage, which is also consistent with the large Ne of C. etunicatum. We propose that in the near absence of recombination, asexual reproduction involving massively multinucleate spores typical for Glomeromycota is responsible for the improved efficacy of selection relative to drift. We postulate that large effective population sizes contribute to the evolutionary longevity of Glomeromycota.