This guest post is by Rebekah Rogers (@evolscientist) on her paper with coauthors “Tandem duplications and the limits of natural selection in Drosophila yakuba and Drosophila simulans” arXived here.
Tandem duplications are widely recognized as a source of genetic novelty. Duplication of gene sequences can result in adaptive evolution through the development of novel functions or specialization in subsets of ancestral functions when ‘spare parts’ are relieved of evolutionary constraints. Additionally, tandem duplications have the potential to create entirely novel gene structures through chimeric gene formation and recruitment of formerly non-coding sequence. Here, we survey the limits of standing variation for tandem duplications in natural populations of D. yakuba and D. simulans, estimate the upper bound of mutation rates, and explore their role in rapid evolution.
Tandem duplicates on the X chromosome in D. simulans show an excess of high frequency variants consistent with adaptive evolution through tandem duplication. Furthermore, we identify an overrepresentation of genes involved in rapidly evolving phenotypes such as chorion development and oogenesis, drug and toxin metabolism, chitin cuticle formation, chemosensory processes, lipases and endopeptidases expressed in male reproduction, as well as immune response to pathogens in both D. yakuba and D. simulans. The enrichment of such rapidly evolving functional classes points to a role for tandem duplicates in Red Queen dynamics and responses to strong selective pressures.
In spite of the observed concordance across functional classes we observe few duplicated genes that are shared across species indicating that parallel recruitment of tandem duplications is rare. The span of duplicates in the population is quite limited, and we estimate that less than 15% of the genome is represented among the tandem duplications segregating in the entire population for the species. Moreover, many duplicates are present at low frequency and will have difficulty escaping the forces of drift during selective sweeps. This very limited standing variation combined with low mutation rates for tandem duplications results in severe limitations in the substrate of genetic novelty that is available for adaptation.
Thus, the limits of standing variation and the rate of new mutations are expected to play a vital role in defining evolutionary trajectories and the ability of organisms to adapt in the event of gross environmental change. Given the limited substrate of genetic novelty, we expect that if adaptation is dependent upon gene duplications, suboptimal outcomes in adaptive walks will be common, long wait times will occur for new phenotypic changes, and many multicellular eukaryotes will display limited ability to adapt to rapidly changing environments.
Haldane's Sieve 
One place I would have liked to see more discussion is on the genetic architecture of traits. One might imagine that for highly quantitative traits populations don’t need to wait for gene duplications, as the mutational target may be quite large and there is likely to be considerable standing genetic variation. For such traits, might we not expect to see repeated evolution (the authors use both “parallel” and “convergent” interchangeably, but I find both terms somewhat confusing and prefer the simpler “repeated”), just not using gene duplications? Then for traits with simpler architectures and a smaller mutational target might gene duplications be expected play a more important role? This idea seems to fit with some of their data — traits where repeated evolution is seen in both taxa include traits such as immunity that may have simple genetic architectures. The authors instead argue that gene duplications may be more important for more quickly evolving phenotypes, but it is not at all clear to me that highly quantitative traits can’t evolve quickly.
In their discussion of repeated evolution between *D. simulans* and *D. yakuba* the authors do not use duplicates fixed within each lineage. If the question is one of repeated evolution between these two taxa, why not include such changes?
In their assessment of the SFS of gene duplicates, the authors make comparisons to putatively neutral intronic SNPs and, upon finding differences, argue that gene duplicates are generally deleterious and of large effect. I would have liked to see comparison to nonsynonymous SNPs as well — do duplicates show a larger skew?
A few minor minor points. The discussion of “convergent” evolution is a bit confusing, as the authors argue in the introduction that it’s the best evidence for natural selection but in the discussion that it’s probably a bad metric. And when discussing the likelihood of adaptation from tandem duplicates the authors cite Haldane’s sieve as a reason why recessive gene duplicates might be less likely to fix, but don’t mention the fact that adaptation from standing variation can change such dynamics.