Inference of chromosomal inversion dynamics fromPool‐Seq data in natural and laboratory populations ofDrosophila melanogaster

Martin Kapun,Thomas Flatt,Christian Schlötterer,Bryant Mcallister,Hester Van Schalkwyk

doi:10.1111/mec.12594

Martin Kapun, Thomas Flatt + Show 3 more

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https://doi.org/10.1111/mec.12594

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Abstract

Sequencing of pools of individuals (Pool-Seq) represents a reliable and cost-effective approach for estimating genome-wide SNP and transposable element insertion frequencies. However, Pool-Seq does not provide direct information on haplotypes so that, for example, obtaining inversion frequencies has not been possible until now. Here, we have developed a new set of diagnostic marker SNPs for seven cosmopolitan inversions in Drosophila melanogaster that can be used to infer inversion frequencies from Pool-Seq data. We applied our novel marker set to Pool-Seq data from an experimental evolution study and from North American and Australian latitudinal clines. In the experimental evolution data, we find evidence that positive selection has driven the frequencies of In(3R)C and In(3R)Mo to increase over time. In the clinal data, we confirm the existence of frequency clines for In(2L)t, In(3L)P and In(3R)Payne in both North America and Australia and detect a previously unknown latitudinal cline for In(3R)Mo in North America. The inversion markers developed here provide a versatile and robust tool for characterizing inversion frequencies and their dynamics in Pool-Seq data from diverse D. melanogaster populations.

Highlights

Inversions are common chromosomal variants of great evolutionary interest; they arise from structural mutations, which cause a reversal of gene order relative to the standard chromosomal arrangement
We identified six polymorphic cosmopolitan inversions segregating in our experimental evolution experiment: four common inversions (In(2L)t, In(2R)Ns, In(3L)P, In(3R)Payne) and two rare cosmopolitan inversions (In(3R)Mo, In(3R)C) (Mettler et al 1977; Lemeunier & Aulard 1992) by cytological analysis of 275 polytene chromosomes from crosses of males with unknown karyotype and females of a noninverted mutant strain
We have presented a novel and robust set of molecular SNP markers for seven polymorphic chromosomal inversions in D. melanogaster, which will be highly useful for the analysis of Pool-Seq data in this model

Summary

Introduction

Inversions are common chromosomal variants of great evolutionary interest; they arise from structural mutations, which cause a reversal of gene order relative to the standard chromosomal arrangement. They have, for example, been found to be involved in sex chromosome evolution (McAllister 2003; Charlesworth et al 2005) and may be key factors for speciation (Noor et al 2001; Rieseberg 2001; Hey 2003; Manoukis et al 2008; Neafsey et al 2010).

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