Evolutionary dynamics of genome size and transposable elements in crickets (Ensifera: Gryllidea)

Abstract

Orthoptera species are characterised by their expansive genomes. However, crickets, the third largest group of this order, have notably smaller genomes than grasshoppers or katydids. The evolutionary drivers behind these differences in genome size (GS) remain largely uncharted. In our study involving 56 cricket species, we assessed GS using flow cytometry and assembled 43 novel mitochondrial genomes for phylogenetic analysis. Model fitting indicated that GS generally conformed to an Ornstein-Uhlenbeck adaptive evolutionary model, displaying a 5.1-fold range of variation in GS, from 0.82 pg in Myrmecophilus quadrispina Perkins to 4.68 pg in Ornebius formosanus Shiraki. Remarkably, despite such variations, no significant trends in genome contraction or expansion were detected, suggesting an adaptive stabilisation. We found strong evidence that expansions of repeat elements, particularly transposable elements (TEs), are key drivers of the large GS in crickets. Across the 56 cricket species analysed, TE content exhibited substantial variability, spanning from a mere 3.63% to a pronounced 31.22%. Clades exhibiting significant GS or TE variations, such as mole crickets (Gryllotalpidae), ant-loving crickets (Myrmecophilidae) and scaly crickets (Mogoplistidae), are often observed at basal phylogenetic nodes and exhibit distinct ecological niches and morphological divergences. This implies that cricket genomes undergo early mutations and stabilise throughout evolution. Our findings shed light on common patterns and uncover lineage-specific differences in content and evolution of TEs in crickets. We anticipate that our study will provide a foundation for future comparative research on the insect TE repertoire.