The evolutionary dynamics of genome sizes and repetitive elements in Ensifera (Insecta: Orthoptera)

BMC Genomics. 2024 Nov 5;25(1):1041. doi: 10.1186/s12864-024-10949-0.

Abstract

Background: In evolutionary biology, identifying and quantifying inter-lineage genome size variation and elucidating the underlying causes of that variation have long been goals. Repetitive elements (REs) have been proposed and confirmed as being among the most important contributors to genome size variation. However, the evolutionary implications of genome size variation and RE dynamics are not well understood.

Results: A total of 35 Ensifera insects were collected from different areas in China, including nine species of crickets and 26 species of katydids. The genome sizes of seven species were then determined using flow cytometry. The RepeatExplorer2 pipeline was employed to retrieve the repeated sequences for each species, based on low-coverage (0.1 X) high-throughput Illumina unassembled short reads. The genome sizes of the 35 Ensifera insects exhibited a considerable degree of variation, ranging from 1.00 to 18.34 pg. This variation was more than 18-fold. Similarly, the RE abundances exhibited considerable variation, ranging from 13.66 to 61.16%. In addition, the Tettigonioidea had larger genomes and contained significantly more REs than did the Grylloidea genomes. Analysis of the correlation between RE abundance and the genome size of 35 Ensifera insects revealed that the abundance of REs, transposable elements (TEs), long terminal repeats (LTRs), and long interspersed nuclear elements (LINEs) are significantly correlated with genome size. Notably, there is an inflection point in this correlation, where species with increasingly large genomes (e.g., > 5-10 pg) have repeats that contribute less to genome expansion than expected. Furthermore, this study revealed contrasting evolutionary directions between the Tettigonioidea and Grylloidea clades in terms of the expansion of REs. Tettigonioidea species exhibit a gradual increase in ancestral genome size and RE abundance as they diverge, while Grylloidea species experience sustained genome contraction.

Conclusions: This study reveals extensive variation in genome size and RE abundance in Ensifera insects, with distinct evolutionary patterns across two major groups, Tettigonioidea and Grylloidea. This provides valuable insights into the variation in genome size and RE abundance in Ensifera insects, offering a comprehensive understanding of their evolutionary history.

Keywords: Ensifera; Genome Size; Repetitive Elements; Transposable Elements.