Evolutionary Dynamics of Transposable Element Activity and Regulation in the Apennine Yellow-Bellied Toad (Bombina pachypus)

Abstract

Transposable elements (TEs) expansion and accumulation represent one of the main drivers of genomic gigantism. Different host genome silencing mechanisms have evolved to counteract TE amplification, leading to a genomic arms race between them. Nevertheless, the evolutionary relationship between TEs and host genome silencing pathways remains poorly understood. Here, we investigate the activity of TEs and TE-silencing mechanisms in somatic and germline tissues of Bombina pachypus, a 10 Gb anuran genome. Our findings reveal a higher activity of TEs in the gonads compared to the brain, with retrotransposons as the most active class in both gonads (∼15% increased expression compared to the brain) and DNA transposons showing a 2-fold higher activity in ovaries. However, analysis of differentially expressed TEs between male and female gonads revealed a greater number of overexpressed TEs in testes (231 vs. 169), with maximum fold changes up to 22 in testes versus 8 in ovaries. This suggests a more permissive environment for TE expression in male gonads. Accordingly, increased activity of TE-silencing pathways was observed in ovaries compared to testes, with the KRAB-ZFP complex showing not only the highest overall expression levels but also a distinct ovary-specific expression pattern. Summarizing, while the higher TE activity in the male gonad may result from the lower efficiency of the KRAB-ZFP complex, the elevated activity of KRAB-ZFPs in ovaries, along with growing evidence of the functional role of TEs in the germline, suggests the existence of a broad range of host-TE dynamics going beyond the arms race model.