A comparative genomic analysis at the chromosomal-level reveals evolutionary patterns of aphid chromosomes

Genomic rearrangements are primary drivers of evolution, promoting biodiversity and differentiation. Aphids, an agricultural pest with high species diversity, exhibit rapid chromosomal evolution and a wide range of nuclear chromosomal karyotype variations. These variations have been attributed to their unique holocentric chromosomes and parthenogenetic generations, though this hypothesis has also faced scrutiny. An in-depth comparative genomics analysis of aphid genomic rearrangements will enhance our understanding of species diversity and evolution. In this study, by generating a chromosomal-level reference genome assembly of the celery aphid (Semiaphis heraclei) and conducting comparative genomic analysis, we revealed varying chromosomal evolution rates among aphid lineages, positively correlating with species diversity. Aphid X chromosomes have undergone frequent intra-chromosomal recombination, while autosomes show accelerated inter-chromosomal recombination. Moreover, considering both inter- and intra-chromosomal rearrangements, the increased autosomal rearrangement rates may be common across the Aphidomorpha lineage. Additionally, the expansion of DNA and SINE-type transposable elements, along with gene loss and duplication associated with karyotypic instability (such as, RIF1, BRD8, DMC1, and TERT), may play crucial roles in aphid chromosomal evolution. Our results provide new insights into aphid chromosomal evolutionary patterns, which are helpful for understanding the genetic mechanisms behind species diversity and adaptive evolution.