DNA methylation reprogramming, TE derepression, and postzygotic isolation of nascent animal species

Abstract

The genomic shock hypothesis stipulates that the stress associated with divergent genome admixture can cause transposable element (TE) derepression, which could act as a postzygotic isolation mechanism. TEs affect gene structure, expression patterns, and chromosome organization and may have deleterious consequences when released. For these reasons, they are silenced by heterochromatin formation, which includes DNA methylation. Here, we show that a significant proportion of TEs are differentially methylated between the "dwarf" (limnetic) and the "normal" (benthic) whitefish, two nascent species that diverged some 15,000 generations ago within the Coregonus clupeaformis species complex. Moreover, TEs are overrepresented among loci that were demethylated in hybrids, indicative of their transcriptional derepression. These results are consistent with earlier studies in this system that revealed TE transcriptional derepression causes abnormal embryonic development and death of hybrids. Hence, this supports a role of DNA methylation reprogramming and TE derepression in postzygotic isolation of nascent animal species.

Fig. 1. Epigenomic and genomic variations between dwarf and normal whitefish species and their reciprocal hybrids.

(A) Principal components analysis (PCA) on 10,374 SNPs. (B) PCA on 423,652 CpGs. (C) Redundancy analysis (RDA) on 10,374 SNPs where genetic variance is explained by the variable lineage. (D) RDA on 423,652 CpGs where epigenetic variance is explained by the variable lineage. Blue circles represent dwarf individuals (DD), red squares represent normal individuals (NN), dark purple down-triangles represent normal ♀-dwarf hybrids (ND), and pale purple up-triangles represent dwarf ♀-normal hybrids (DN). (E) Distribution of CpG according to their methylation level for pure and hybrid whitefish groups represented by the same color used above. (F) Pairwise individual correlation between CpG methylation levels. The tree was constructed using UPGMA methods, and the correlation matrix of level of methylation was observed among individuals.

Fig. 2. DNA methylation differentiation between dwarf and normal whitefish species and their reciprocal hybrids.

Methylation differentiation between pure dwarf and normal whitefish species (top panels) and between parental species and their hybrids (bottom panels). (A and B) Histograms representing the distribution of loci differentially methylated based on how many differently methylated CpGs (>20%) they harbor. Red and blue coloration represent hyper- and hypomethylation in dwarf in comparison to normal (A) and hybrids in comparison to parental lineages (B), respectively. (C and D) Heatmaps of differentially methylated CpGs (>20%) separated in four k-means groups that separated pure species (C) and pure species from hybrids (D). TE enrichment (FDR < 0.05) for each CpG category is provided at the right of each heatmap.

Fig. 3. Transposable element annotation and their proportions of DNA methylation differentiation between dwarf and normal whitefish species.

(A) Pie chart of annotated TEs in the transcriptome for all TEs, LTR retrotransposons, non-LTR retrotransposons, and transposons. (B) Proportion of transcripts harboring at least one CpG differently methylated in the entire transcriptome, in all transcripts annotated as TEs, in all transcripts annotated as a Gypsy TE superfamily, in addition to REX, Tc1-Mariner, and L2 superfamilies.