Comparative analysis reveals within-population genome size variation in a rotifer is driven by large genomic elements with highly abundant satellite DNA repeat elements

C P Stelzer,A M Waldvogel,D B Mark Welch,M Pichler,J Blommaert,J Blommaert,B Hecox-Lea

doi:10.1186/s12915-021-01134-w

C P Stelzer, A M Waldvogel + Show 5 more

Open Access

https://doi.org/10.1186/s12915-021-01134-w

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Abstract

BackgroundEukaryotic genomes are known to display an enormous variation in size, but the evolutionary causes of this phenomenon are still poorly understood. To obtain mechanistic insights into such variation, previous studies have often employed comparative genomics approaches involving closely related species or geographically isolated populations within a species. Genome comparisons among individuals of the same population remained so far understudied—despite their great potential in providing a microevolutionary perspective to genome size evolution. The rotifer Brachionus asplanchnoidis represents one of the most extreme cases of within-population genome size variation among eukaryotes, displaying almost twofold variation within a geographic population.ResultsHere, we used a whole-genome sequencing approach to identify the underlying DNA sequence differences by assembling a high-quality reference genome draft for one individual of the population and aligning short reads of 15 individuals from the same geographic population including the reference individual. We identified several large, contiguous copy number variable regions (CNVs), up to megabases in size, which exhibited striking coverage differences among individuals, and whose coverage overall scaled with genome size. CNVs were of remarkably low complexity, being mainly composed of tandemly repeated satellite DNA with only a few interspersed genes or other sequences, and were characterized by a significantly elevated GC-content. CNV patterns in offspring of two parents with divergent genome size and CNV patterns in several individuals from an inbred line differing in genome size demonstrated inheritance and accumulation of CNVs across generations.ConclusionsBy identifying the exact genomic elements that cause within-population genome size variation, our study paves the way for studying genome size evolution in contemporary populations rather than inferring patterns and processes a posteriori from species comparisons.

Highlights

Eukaryotic genomes are known to display an enormous variation in size, but the evolutionary causes of this phenomenon are still poorly understood
De novo assembly and annotation of the reference genome The rotifer clone (OHJ7i3n10) chosen for our reference genome derives from the natural isolate OHJ7 after three rounds of selfing
Most hits could correctly be assigned to rotifers and remaining hits assigned to mollusks and arthropods can mostly be explained by imbalanced availability of rotifer entries in the nt database (Additional file 1: Figure S2, Additional file 2)

Summary

Introduction

Eukaryotic genomes are known to display an enormous variation in size, but the evolutionary causes of this phenomenon are still poorly understood. Much of our understanding of eukaryotic genome size variation comes from comparisons between closely related species. It was possible to pinpoint individual REs as the driver of genome expansion [10, 11], whereas in other studies, differently sized genomes were found to differ in several classes of REs [12, 13] In the latter case, it is difficult to decide whether multiple RE classes have expanded more or less simultaneously in evolutionary time, or whether the expansions of some REs have occurred after an initial genome size divergence driven by a single element. Identifying genome size variants within populations and studying them on microevolutionary time scales may allow additional insights into the evolutionary dynamics of early genome divergences

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