Discovery and population genomics of structural variation in a songbird genus

Matthias H Weissensteiner,Alexander Suh,Ignas Bunikis,Fritz J Sedlazeck,Saurabh D Pophaly,Wieland Heim,Ana Catalán,Jochen B W Wolf,Valentina Peona,Vera M Warmuth,Kees-Jan Francoijs,Ulrich Knief

doi:10.1038/s41467-020-17195-4

Abstract

Structural variation (SV) constitutes an important type of genetic mutations providing the raw material for evolution. Here, we uncover the genome-wide spectrum of intra- and interspecific SV segregating in natural populations of seven songbird species in the genus Corvus. Combining short-read (N = 127) and long-read re-sequencing (N = 31), as well as optical mapping (N = 16), we apply both assembly- and read mapping approaches to detect SV and characterize a total of 220,452 insertions, deletions and inversions. We exploit sampling across wide phylogenetic timescales to validate SV genotypes and assess the contribution of SV to evolutionary processes in an avian model of incipient speciation. We reveal an evolutionary young (~530,000 years) cis-acting 2.25-kb LTR retrotransposon insertion reducing expression of the NDP gene with consequences for premating isolation. Our results attest to the wealth and evolutionary significance of SV segregating in natural populations and highlight the need for reliable SV genotyping.

Highlights

Structural variation (SV) constitutes an important type of genetic mutations providing the raw material for evolution
The genetic basis of plumage variation and its contribution to population divergence has been investigated in much detail using single-nucleotide polymorphism (SNP) data in the Corvus spp. species complex that is characterized by narrow contact zones between all-black forms (C. (c.) corone/ orientalis) and populations consisting of the pied phenotype (C. (c.) cornix/capellanus/pallescens/pectoralis/sharpii)[20,21,22]
We first generated high-quality phased de novo genome assemblies combining long-read (LR) data from single-molecule, real-time (SMRT, PacBio) sequencing, and nanochannel optical mapping (OM) for the hooded crow (Corvus cornix; data from Weissensteiner et al.28), and the European jackdaw (Corvus monedula, this study)

Summary

Introduction

Structural variation (SV) constitutes an important type of genetic mutations providing the raw material for evolution. Despite some indication for a structural rearrangement underlying phenotypic divergence in two European crow populations[24], the overall extent and role of SV in population divergence remains unclear in this system To fill this gap and more broadly investigate the dynamics of SV in natural populations, we compiled short-read, long-read, and optical mapping data for populations of seven species from the genus Corvus. We generated genome assemblies for two of the species spanning the evolutionary history of the clade, comprehensively characterized SV using read-mapping and assembly-based approaches and used phylogenetically informed filtering to obtain reliable SV genotypes After establishing these genomic resources, we demonstrated the suitability of SV for population genetic analysis and evolutionary inference using the Corvus (corone) spp. species complex

Methods

Results

Conclusion