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

Abstract

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 summary 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.

Adding New Pieces to the Puzzle of Karyotype Evolution in Harttia (Siluriformes, Loricariidae): Investigation of Amazonian Species

“…Taking an important role in the initial steps of sex chromosome differentiation, in post-zygotic reproductive isolation, or by contributing to local adaptation in certain populations, chromosomal inversions can suppress the recombination, especially around the rearrangement breakpoints [ 69 , 70 , 71 , 72 , 73 , 74 , 75 , 76 , 77 ]. In addition, repetitive DNAs may also play an important role in promoting biodiversity, in the differentiation of sex-specific chromosomal regions, and speciation of diverse eukaryotic organisms including fishes [ 78 , 79 , 80 , 81 ]. As evidenced in our present study, the differences in karyotype organization and number and distribution of rDNA sites are instrumental as chromosomal markers for the determination of Harttia species with 2n = 54 chromosomes.…”

Bacterial N4-methylcytosine as an epigenetic mark in eukaryotic DNA

“…Notably, bdelloids exhibit some of the lowest TE content among metazoans, while members of their sister class Monogononta, which lack cytosine methylation and encode a single SETDB1 copy, show reduced ability to contain TE proliferation, which can double their genome size 67 . Earlier, we found a drastic expansion of Ago/Piwi and RdRP proteins in bdelloids, which are very TE-poor, in contrast to the acanthocephalan Pomphorhynchus laevis (Rotifera) with 66% TE content and no expansion of Ago/Piwi 16,47 , underscoring the importance of RNA silencing pathways in TE control.…”

Within-population genome size variation is mediated by multiple genomic elements that segregate independently during meiosis

“…Indeed, preliminary comparisons among clones of the selfed lines confirm that large genomic regions (spanning multiple Mbp in size) are entirely missing in a clone with the minimal genome size (~414 Mbp), and that the same regions have high and variable coverage in clones with larger genome sizes, at coverage ratios consistent with the number of independently segregating elements (Blommaert et al unpublished). Also recently, we have compared the genome architecture of B. asplanchnoidis to that of other species of the B. plicatilis species complex and found that transposable element abundance rather than an allopolyploid origin explains the large genome size of B. asplanchnoidis (36). Even though B. asplanchnoidis has a relatively small genome compared to other metazoans, it has a strikingly high repetitive element content of 44%.…”