Extreme genome scrambling in crypticOikopleura dioicaspecies

Abstract

Genes are not randomly distributed throughout chromosomes. How gene order evolves and how selective constraints act to preserve or vary gene order, both at the macrosyntenic level of whole chromosomes or microsyntenic level of gene blocks, are central questions of evolutionary biology and genomics that remain largely unsolved. Here, after sequencing several genomes of the appendicularian tunicate Oikopleura dioica from different locations around the globe, we show an unprecedented amount of genome scrambling in animals with no obvious morphological differences, consistent with cryptic speciation. Our assemblies suggest that all members of this clade possess a common 3-chromosome karyotype, and that different species largely preserve gene content, despite the presence of thousands of rearrangements in gene order. The movements of genes are largely restricted to chromosome arms and sex-specific regions, which appear to be the primary unit of macrosynteny conservation, and examples of these within-arm movements can be seen in the Hox and Fgf gene families. Our approach employing whole-genome alignments demonstrates that segments containing protein-coding elements tend to be preserved at the microsyntenic scale, consistent with strong purifying selection, with appreciably less preservation of non-coding elements. Unexpectedly, scrambling did not preserve operon structure across species, suggesting an absence of selective pressure to maintain operon structure. As well, genome scrambling does not occur uniformly across all chromosomes, as short chromosome arms possess shorter genes, smaller operons, more breakpoints, and elevated dN/dS values compared to long chromosome arms. Estimation of divergence times among the cryptic O. dioica lineages yielded an estimated breakpoint accumulation rate of 6 to 25 breakpoints per megabase per million years, which is an order of magnitude higher than the rates for other ascidian tunicates or Drosophila species. Therefore, O. dioica appears to be an attractive animal system to unravel the mechanisms that underlie gene order and synteny conservation, as well as exploring the limits of genome scrambling without an apparent impact on phenotypic evolution.

First chromosome-level genome assembly of the colonial tunicateBotryllus schlosseri

“…The comparison with Oikopleura dioica showed a complete loss of both synteny and colinearity due to chromosome fission and extreme mixing. The latter result is in line with the very long and fast-evolving branch of the Appendicularia when compared to the other tunicates (48) as well as an extreme genome scrambling rate of Appendicularia compared to other tunicates and mammals (51). The same analyses using a set of 29 linkage groups generally conserved among bilaterians (52) yielded similar results (not shown).…”

A comparative analysis of planarian genomes reveals regulatory conservation in the face of rapid structural divergence

“…3B) and the finding that 80% of our enhancer annotations in the S. mediterranea genome are located in introns, exons, or within 1 kb of the closest gene body (Fig. 2G, Additional File 1: Section 2.3), may reflect a particularly tight association of regulatory elements with their target genes (a genome architecture similar to a tunicate species complex with rapid chromosome-arm restricted gene shuffling 79 ). However, cell or tissue type-specific Hi-C data sets and quantitative comparisons of enhancer distributions with well-annotated genomes will be required to understand the extend by which these observation reflect technical artefacts versus genuine mechanistic differences in the control of gene expression in planarians.…”

Fusion, fission, and scrambling of the bilaterian genome in Bryozoa

“…Species from phyla as divergent as chordates, echinoderms, molluscs, and annelids have largely retained these highly-conserved bilaterian blocks of genes (4,6,(11)(12)(13), suggesting substantial functional constraints. There are lineages within phyla that have experienced genomic shuffling, such as planarians (14) and tunicates (15), but conservation of the ALGs seems the norm at the phylum level. Despite this conservation, fluctuation in chromosome number is a relatively frequent evolutionary process (16)(17)(18)(19).…”