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

BACKGROUND: Eukaryotic 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. RESULTS: Here, 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. CONCLUSIONS: By 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.

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

BACKGROUND: 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. 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). RESULTS: Despite 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. CONCLUSIONS: Even 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.