Transposable elements and polyploid evolution in animals

Abstract

Polyploidy in animals is much less common than in plants, where it is thought to be pervasive in all higher plant lineages. Recent studies have highlighted the impact of polyploidization and the associated process of diploidy restoration on the evolution and speciation of selected taxonomic groups in the animal kingdom: from vertebrates represented by salmonid fishes and African clawed frogs to invertebrates represented by parasitic root-knot nematodes and bdelloid rotifers. In this review, we focus on the unique and diverse roles that transposable elements may play in these processes, from marking and diversifying subgenome-specific chromosome sets before hybridization, to influencing genome restructuring during rediploidization, to affecting subgenome-specific regulatory evolution, and occasionally providing opportunities for domestication and gene amplification to restore and improve functionality. There is still much to be learned from the future comparative genomic studies of chromosome-sized and haplotype-aware assemblies, and from postgenomic studies elucidating genetic and epigenetic regulatory phenomena across short and long evolutionary distances in the metazoan tree of life.

Figure 1

Transposable elements and representative species discussed in the text. (a) A compilation of major structural features for class I TE (retrotransposons) and class II TE (DNA transposons). Shown are the characteristic ORFs with functional domains (RT, reverse transcriptase; IN, integrase; PR, protease; EN, endonuclease; PolB, family B DNA polymerase; DJR, double jelly-roll capsid-like protein) and direct or inverted repeats or poly-A stretches at the termini. Selected representatives, including those mentioned in the text and figures, are listed in parentheses. Not to scale. (b) Phylogenetic relationships in teleost fish and the ancestral spotted gar, with salmonids shown in red (after ref. [15]). Yellow and red circles represent the teleost-specific whole genome duplication (Ts3R) and the salmonid-specific whole genome duplication (Ss4R), respectively. (c) Phylogeny of Xenopus frogs according to [22]. Hybridization between the progenitor Xenopus-L and Xenopus-S species is denoted by purple star. Estimated peaks of L-harbinger and S-mariner activity are shown at 33–34 Mya and 18 Mya, respectively. (d) A consensus phylogram illustrating relationships between root-knot nematodes discussed in the text, based on [–26]. Species with elevated ploidy are shown in green; the green star denotes the presumed recent hybridization(s), the precise time estimate for which was not reported. M. javanica is shown as a polytomy, since its phylogenetic placement differs in [24] and [26]. In (b-d), the cases of ploidy increase are shown by colored lines with double thickness.

Figure 2

TE class abundance and diversity in selected polyploid animal species A. vaga, M. arenaria, M. incognita, M. javanica, X. laevis, O. mykiss and S. salar, discussed in the text. For comparison, the diploid species M. hapla, L. oculatus and X. tropicalis are included. (a) Histogram of TE content profile. The X-axis shows the percentage of the genome assembly occupied by each TE class/order, as specified in the legend. “Other” denotes unclassified repeats. (b) Relationship between TE content and genome size. Content is given as the percentage of coverage of the genome assembly by retrotransposons (X-axis) and DNA transposons (Y-axis). The area of each bubble representing a species is proportional to its genome size (Mb): M. hapla (53.6), M. incognita (183.5), A. vaga (213.8), M. javanica (235.8), M. arenaria (258), L. oculatus (945), X. tropicalis (1513), O. mykiss (1877.5), X. laevis (2408.8) and S. salar (2970). Data sources: [15,17,18,22,24,29,44].

Figure 3

A compilation of TE divergence plots over the evolutionary time scales in selected fish genomes discussed in the text. The S. salar plot (a) shows Tc1-like DNA TEs, with the X-axis showing per cent similarity to the consensus for each family and the Y-axis showing its genome abundance in Mb [15]. The O. mykiss (b) [17] and L. oculatus (c) [18] panels show the canonical RepeatMasker [45] TE landscape divergence plots with Kimura distances on the X-axis and per cent of the genome occupied by each TE superfamily on the Y-axis. The scales on the X-axes differ for (a) vs (b) and (c), thus the S. salar plot was mirrored and stretched to extend the X scale to the limit of detection beyond which no data can be plotted (25% nucleotide divergence, or Kimura distances of 50). Arrows indicate major TE expansions.