Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate

Abstract

Genomes of animals as different as sponges and humans show conservation of global architecture. Here we show that multiple genomic features including transposon diversity, developmental gene repertoire, physical gene order, and intron-exon organization are shattered in the tunicate Oikopleura, belonging to the sister group of vertebrates and retaining chordate morphology. Ancestral architecture of animal genomes can be deeply modified and may therefore be largely nonadaptive. This rapidly evolving animal lineage thus offers unique perspectives on the level of genome plasticity. It also illuminates issues as fundamental as the mechanisms of intron gain.

Fig. 1

Genome compaction features. (A) Chromosome regions assembled with physical links and genetic markers. The location of TEs is indicated with horizontal lines (lines on the left sides, DNA transposons; lines on right sides, short lines for long terminal repeat–retrotransposons and long lines for long interspersed elements). (B) Distribution of gene models over 10% abundance classes of intron size and upstream intergenic distance for 8812 nonoperon genes (left) and for 189 developmentally regulated genes, mainly transcription factors (right). (C) Conserved elements revealed in genome alignments of Atlantic and Pacific ocean populations of O. dioica:density of conserved blocks (top), gene annotation (middle), and perfectly conserved elements >100 bp (bottom gray line) (blue, Norway versus northwest America; red, Norway versus Japan). (D) Giant Y genes and their testis expression revealed by reverse transcription polymerase chain reaction and in situ hybridization. hpf, hours post fertilization; ctrl, control. The arrowhead indicates the giant gene expression product.

Fig. 2

Introns and intron gain scenarios. (A) Main intron logos. (B) Transposon insertion: Duplicated insertion sites (framed in blue) allow miniature inverted repeat transposable element (MITE)–like insertions to be spliced out exactly (red, exons; black, introns). (C) Reverse splicing: four pairs of homologous introns (black) and their immediate exonic environments (red).

Fig. 3

Gene duplications and loss of ancestral syntenies. (A) Early gene duplicates. (Main panel) Histogram of binned recent duplicate pairs; a mixture model (discrete distribution plus truncated Weibull distributions) accommodating heterogeneous birth/death processes is fitted. (Inset) Non-synonymous substitution accumulation declines with ongoing synonymous substitution. (B) Expression of amplified homeobox gene groups in the trunk epithelium of larvae (red arrowheads). hD, hours dorsal view; hL, hours lateral view; hDL, hours dorsolateral view. (C) Loss of ancestral gene order. Positions of orthologous genes in a given metazoan genome (y axis) compared with ancestral chordate linkage groups [(CLGs), x axis]. The width of CLGs corresponds to the number of orthologs in a given species. Amphioxus and sea anemone genome segments represent the largest 25 assembled scaffolds, whereas Ciona, nematode, and Oikopleura segments are chromosomes.