Rapid Increase in frequency of gene copy-number variants during experimental evolution in Caenorhabditis elegans.

James C. Farslow,Donald G. Moerman,Lucille B. Packard,Mark L. Edgley,Stephane Flibotte,Ulfar Bergthorsson,Kendra J. Lipinski,Jon Taylor,Vaishali Katju

doi:10.1186/s12864-015-2253-2

Abstract

BackgroundGene copy-number variation (CNVs), which provides the raw material for the evolution of novel genes, is widespread in natural populations. We investigated whether CNVs constitute a common mechanism of genetic change during adaptation in experimental Caenorhabditis elegans populations. Outcrossing C. elegans populations with low fitness were evolved for >200 generations. The frequencies of CNVs in these populations were analyzed by oligonucleotide array comparative genome hybridization, quantitative PCR, PCR, DNA sequencing across breakpoints, and single-worm PCR.ResultsMultiple duplications and deletions rose to intermediate or high frequencies in independent populations. Several lines of evidence suggest that these changes were adaptive: (i) copy-number changes reached high frequency or were fixed in a short time, (ii) many independent populations harbored CNVs spanning the same genes, and (iii) larger average size of CNVs in adapting populations relative to spontaneous CNVs. The latter is expected if larger CNVs are more likely to encompass genes under selection for a change in gene dosage. Several convergent CNVs originated in populations descended from different low fitness ancestors as well as high fitness controls.ConclusionsWe show that gene copy-number changes are a common class of adaptive genetic change. Due to the high rates of origin of spontaneous duplications and deletions, copy-number changes containing the same genes arose readily in independent populations. Duplications that reached high frequencies in these adapting populations were significantly larger in span. Many convergent CNVs may be general adaptations to laboratory conditions. These results demonstrate the great potential borne by CNVs for evolutionary adaptation.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-2253-2) contains supplementary material, which is available to authorized users.

Highlights

Gene copy-number variation (CNVs), which provides the raw material for the evolution of novel genes, is widespread in natural populations
The mean productivity of the five focal mutation accumulation (MA) lines at the termination of the MA l phase (50 MA generations) was 31 offspring and the individual mean productivity of the five experimental MA lines ranged from 2–60 progeny
Several lines of evidence suggest that the high frequency of copy-number changes in the adaptive recovery and control populations are primarily due to natural selection

Summary

Introduction

Gene copy-number variation (CNVs), which provides the raw material for the evolution of novel genes, is widespread in natural populations. The rates of spontaneous gene duplication and deletion are extraordinarily high and speak to the enormous potential of these structural variants for generating new adaptive variability [5,6,7,8,9,10]. Ohno [1] theorized that newly duplicated genes were freed from the constraints of natural selection, implicating a dominant role of genetic drift in their early evolutionary dynamics. Farslow et al BMC Genomics (2015) 16:1044 selection for increased gene expression may represent an important mechanism by which duplicate gene copies are maintained in populations [14]. There is ample evidence for the preservation of multiple gene copies due to selection for increased gene dosage in diverse organisms [20]. Gene loss has been associated with adaptation in diverse systems [45,46,47]

Methods

Results

Discussion

Conclusion