Tandem Duplications and the Limits of Natural Selection in Drosophila yakuba and Drosophila simulans.

TitleTandem Duplications and the Limits of Natural Selection in Drosophila yakuba and Drosophila simulans.
Publication TypeJournal Article
Year of Publication2015
AuthorsRogers, RL, Cridland, JM, Shao, L, Hu, TT, Andolfatto, P, Thornton, KR
JournalPLoS One
Volume10
Issue7
Paginatione0132184
Date Published2015
ISSN1932-6203
KeywordsAnimals, Biological Evolution, Drosophila, Drosophila simulans, Gene Duplication, Genetic Variation, Genome, Insect, Likelihood Functions, Polymorphism, Single Nucleotide, Selection, Genetic, X Chromosome
Abstract

<p>Tandem duplications are an essential source of genetic novelty, and their variation in natural populations is expected to influence adaptive walks. Here, we describe evolutionary impacts of recently-derived, segregating tandem duplications in Drosophila yakuba and Drosophila simulans. We observe an excess of duplicated genes involved in defense against pathogens, insecticide resistance, chorion development, cuticular peptides, and lipases or endopeptidases associated with the accessory glands across both species. The observed agreement is greater than expectations on chance alone, suggesting large amounts of convergence across functional categories. We document evidence of widespread selection on the D. simulans X, suggesting adaptation through duplication is common on the X. Despite the evidence for positive selection, duplicates display an excess of low frequency variants consistent with largely detrimental impacts, limiting the variation that can effectively facilitate adaptation. Standing variation for tandem duplications spans less than 25% of the genome in D. yakuba and D. simulans, indicating that evolution will be strictly limited by mutation, even in organisms with large population sizes. Effective whole gene duplication rates are low at 1.17 × 10-9 per gene per generation in D. yakuba and 6.03 × 10-10 per gene per generation in D. simulans, suggesting long wait times for new mutations on the order of thousands of years for the establishment of sweeps. Hence, in cases where adaptation depends on individual tandem duplications, evolution will be severely limited by mutation. We observe low levels of parallel recruitment of the same duplicated gene in different species, suggesting that the span of standing variation will define evolutionary outcomes in spite of convergence across gene ontologies consistent with rapidly evolving phenotypes. </p>

DOI10.1371/journal.pone.0132184
Alternate JournalPLoS ONE
PubMed ID26176952
PubMed Central IDPMC4503668
Grant ListF32-GM099377 / GM / NIGMS NIH HHS / United States
R01-GM083228 / GM / NIGMS NIH HHS / United States
R01 GM085183 / GM / NIGMS NIH HHS / United States
GM085183 / GM / NIGMS NIH HHS / United States
P30CA062203 / CA / NCI NIH HHS / United States