Small, but surprisingly repetitive genomes: transposon expansion and not polyploidy has driven a doubling in genome size in a metazoan species complex

J Blommaert,C P Stelzer,B Hecox-Lea,D B Mark Welch,S Riss

doi:10.1186/s12864-019-5859-y

J Blommaert, C P Stelzer + Show 3 more

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https://doi.org/10.1186/s12864-019-5859-y

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Journal: BMC Genomics	Publication Date: Jun 7, 2019
Citations: 39	License type: open-access

Affiliation: Universität Innsbruck, Marine Biological Laboratory

Abstract

BackgroundThe causes and consequences of genome size variation across Eukaryotes, which spans five orders of magnitude, have been hotly debated since before the advent of genome sequencing. Previous studies have mostly examined variation among larger taxonomic units (e.g., orders, or genera), while comparisons among closely related species are rare. Rotifers of the Brachionus plicatilis species complex exhibit a seven-fold variation in genome size and thus represent a unique opportunity to study such changes on a relatively short evolutionary timescale. Here, we sequenced and analysed the genomes of four species of this complex with nuclear DNA contents spanning 110–422 Mbp. To establish the likely mechanisms of genome size change, we analysed both sequencing read libraries and assemblies for signatures of polyploidy and repetitive element content. We also compared these genomes to that of B. calyciflorus, the closest relative with a sequenced genome (293 Mbp nuclear DNA content).ResultsDespite the very large differences in genome size, we saw no evidence of ploidy level changes across the B. plicatilis complex. However, repetitive element content explained a large portion of genome size variation (at least 54%). The species with the largest genome, B. asplanchnoidis, has a strikingly high 44% repetitive element content, while the smaller B. plicatilis genomes contain between 14 and 25% repetitive elements. According to our analyses, the B. calyciflorus genome contains 39% repetitive elements, which is substantially higher than previously reported (21%), and suggests that high repetitive element load could be widespread in monogonont rotifers.ConclusionsEven though the genome sizes of these species are at the low end of the metazoan spectrum, their genomes contain substantial amounts of repetitive elements. Polyploidy does not appear to play a role in genome size variations in these species, and these variations can be mostly explained by changes in repetitive element content. This contradicts the naïve expectation that small genomes are streamlined, or less complex, and that large variations in nuclear DNA content between closely related species are due to polyploidy.

Highlights

The causes and consequences of genome size variation across Eukaryotes, which spans five orders of magnitude, have been hotly debated since before the advent of genome sequencing
These studies exemplify how the comparison of genome size and genomic composition across broad evolutionary scales can illuminate the causes of genome size variation, and highlight that polyploidy is often implicated in large genome size changes within or between closely related species, while repetitive elements tend to be linked with smaller or more gradual changes in genome size
The number of sequenced base pairs ranged from 2.06 Gigabase pairs (Gbp) to 9.77 Gbp; we identified 0.4–8% of reads as coming from contaminants, and retained between 2.01 and 9.73 Gbp

Summary

Introduction

The causes and consequences of genome size variation across Eukaryotes, which spans five orders of magnitude, have been hotly debated since before the advent of genome sequencing. We sequenced and analysed the genomes of four species of this complex with nuclear DNA contents spanning 110–422 Mbp. To establish the likely mechanisms of genome size change, we analysed both sequencing read libraries and assemblies for signatures of polyploidy and repetitive element content. Other examples include genome size change in a clade of butterflies caused by an increase in transposable elements [18], and analyses of variation in the composition of B-chromosomes in grasshoppers [19,20,21] These studies exemplify how the comparison of genome size and genomic composition across broad evolutionary scales can illuminate the causes of genome size variation, and highlight that polyploidy is often implicated in large genome size changes within or between closely related species, while repetitive elements tend to be linked with smaller or more gradual changes in genome size

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