Abstract

One common hypothesis to explain the impacts of tandem duplications is that whole gene duplications commonly produce additive changes in gene expression due to copy number changes. Here, we use genome wide RNA-seq data from a population sample of Drosophila yakuba to test this ‘gene dosage’ hypothesis. We observe little evidence of expression changes in response to whole transcript duplication capturing 5′ and 3′ UTRs. Among whole gene duplications, we observe evidence that dosage sharing across copies is likely to be common. The lack of expression changes after whole gene duplication suggests that the majority of genes are subject to tight regulatory control and therefore not sensitive to changes in gene copy number. Rather, we observe changes in expression level due to both shuffling of regulatory elements and the creation of chimeric structures via tandem duplication. Additionally, we observe 30 de novo gene structures arising from tandem duplications, 23 of which form with expression in the testes. Thus, the value of tandem duplications is likely to be more intricate than simple changes in gene dosage. The common regulatory effects from chimeric gene formation after tandem duplication may explain their contribution to genome evolution.

Highlights

  • Tandem duplications are known as a source of genetic novelty that can contribute new genes with novel functions [1, 2]

  • The enclosed work shows that whole gene duplications rarely affect gene expression, in contrast to widely held views that the adaptive value of duplicate genes is related to additive changes in gene expression due to gene copy number

  • We further explain how tandem duplications that create shuffled gene structures can force upregulation of gene sequences, de novo gene creation, and multifold changes in transcript levels. These results show that tandem duplications can produce new genes that are a source of immediate novelty associated with more extreme expression changes than previously suggested by theory

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Summary

Introduction

Tandem duplications are known as a source of genetic novelty that can contribute new genes with novel functions [1, 2]. In spite of the many case studies showing adaptive changes, theoretical arguments suggested that functional divergence would be difficult to attain via whole gene duplication [7]. Loss appears to be the prevailing fate of duplicate and chimeric genes [8, 7, 9] This observed contradiction between the role of duplicates in adaptive evolution and models that led to their erosion of genes from the genome was perceived at the time as a problem for duplicate gene theory. How might these duplicate genes with novel functions accumulate if loss was swift and functional divergence was slow?

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