Investigating the Impact of Whole-Genome Duplication on Transposable Element Evolution in Teleost Fishes

Abstract

Transposable elements (TEs) can make up more than 50% of any given vertebrate's genome, with substantial variability in TE composition among lineages. TE variation is often linked to changes in gene regulation, genome size, and speciation. However, the role that genome duplication events have played in generating abrupt shifts in the composition of the mobilome over macroevolutionary timescales remains unclear. We investigated the degree to which the teleost genome duplication (TGD) shaped the diversification trajectory of the teleost mobilome. We integrate a new high coverage genome of Polypterus bichir with data from over 100 publicly available actinopterygian genomes to assess the macroevolutionary implications of genome duplication events on TE evolution in teleosts. Our results provide no evidence for a substantial shift in mobilome composition following the TGD event. Instead, the diversity of the teleost mobilome appears to have been shaped by a history of lineage-specific shifts in composition that are not correlated with commonly evoked drivers of diversification such as body size, water column usage, or latitude. Collectively, these results provide additional evidence for an emerging perspective that TGD did not catalyze bursts of diversification and innovation in the actinopterygian mobilome.

Keywords: Actinopterygii; Teleostei; living fossil; teleost genome duplication; transposable elements.

Fig. 1.

Major patterns of TE evolution across the evolutionary history of ray-finned fishes. a) The relative abundance of DNA, LTR, LINE, SINE transposons, and unknown transposons relative to actinopteryigiian phylogeny are shown. b) Total TE % and absolute genome size in the context of evolutionary history are compared. c) Results of a phylogenetic generalized least-squares regression to assess the relationship between genome size and TE abundance are provided. d) TE % and genome size between teleosts and nonteleost actinopterygians are compared. Shadings in (a) correspond to elements labeled in the panel. Shadings in (b) correspond to high (light or dark) and low values (dark or light) in the upper and lower panels, respectively. Shadings in (c) correspond to the labels in (a) for individual elements. Panels in (d) correspond to the quantiles of each category with dark horizontal lines indicating the mean value.

Fig. 2.

Correlation between relative class I and class II mobilome content. Panels a), b), and c) display the correlations between DNA transposons and LINE, LTR, and SINE transposons resulting from phylogenetic generalized least-squares regressions, respectively. Panels d) and e) illustrate the correlations based on a phylogenetic generalized least squares regression between LTR transposons and LINE and SINE transposons, respectively. Panel f) presents the correlation based on a phylogenetic generalized least-squares regression between LINE and SINE transposons.

Fig. 3.

Reconstructing the ancestral actinopterygian mobilome. The presence and absence of TE superfamilies (listed above) are represented by blue and gray squares, respectively, for various species on the left (top panel). The shaded area behind the fish paintings represents teleosts, while the unshaded region below represents nonteleosts with evolutionary relationships between taxa depicted by the phylogenetic tree on the far-left. These input data were used to estimate the ancestral mobilome (the probability of each TE superfamily being present or absent) for the most recent common ancestor of all Actinopterygii (A), Neopterygii (N), or Teleostei (T) using SIMMAP (bottom panel). With a resulting heatmap plotted using ggplot (Wickham 2016).

Fig. 4.

Correlation of TEs with biotic and abiotic factors. a) This panel displays the results of phylogenetic generalized least-squares (PGLS) regressions between TE percentages and median latitude b) This panel portrays the PGLS regression results between TE percentage and body size (log-transformed). Lastly, c) depicts PGLS results between TE abundance and the maximum habitat depth of the species. The colors and shapes of each data point on the plot are defined in the key.

Fig. 5.

Considering TE diversity in the context of evolutionary history. a) Results of a Phylogenetic PCA on the abundances of LTRs, DNA transposons, LINEs, and SINEs that project the phylogeny and points onto a 2D plot of PC1 and PC2. b) Depicts the resulting space based on the residual variation following linear regression between major TE classes and genome size. c) Depicts the results of a PCA on the residual variation of the abundances of all 25 superfamilies accounting for differences in genome size, consisting of 13 DNA transposons, 7 LINEs, and 5 LTR subfamilies. Dark shading indicates nonteleost actinopterygians; light shading indicates teleosts. All the images of the fishes are from Wikimedia commons.