Tandem duplications and the limits of natural selection in Drosophila yakuba and Drosophila simulans

TL;DR

This study investigates the evolutionary role of tandem duplications in Drosophila yakuba and Drosophila simulans, revealing their contribution to adaptation, rapid evolution, and the limitations imposed by mutation rates and standing variation.

Contribution

It provides the first comprehensive analysis of segregating tandem duplications in natural Drosophila populations, highlighting their functional roles and evolutionary constraints.

Findings

Duplications are enriched in genes related to defense, resistance, and development.

Evidence of positive selection on the D. simulans X chromosome.

Duplication rates are low, limiting rapid adaptation through new mutations.

Abstract

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, suggesting that duplications function in Red Queen dynamics and rapid evolution. 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. Although we observe hundreds of gene duplications, we show that segregating variation is insufficient to provide duplicate copies of the entire genome, and the number of duplications in the population spans 13.4\% of major chromosome arms in D. yakuba and 9.7\% in D. simulans. Whole gene duplication rates are low at $1.17\times10^{-9}$ per gene per generation in D. yakuba and $6.03\times10^{-10}$ 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 adaption 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.} }