Chromosome-Level Genome Assembly of Apoderus dimidiatus Voss (Coleoptera: Attelabidae): Insights into Evolution and Behavior

TL;DR

This study provides a high-quality genome for the leaf-rolling weevil A. dimidiatus, revealing genetic factors behind its unique behavior and evolutionary history.

Contribution

The first chromosome-level genome assembly of A. dimidiatus, offering insights into gene families linked to leaf rolling behavior and evolutionary divergence.

Findings

Expanded gene families in A. dimidiatus are linked to water balance and skin regulation, crucial for survival in leaf rolls.

Contracted gene families are associated with protease activity and transmembrane transport, affecting offspring survival and egg production.

Phylogenetic analysis shows Attelabidae diverged from Curculionidae about 161.52 million years ago.

Abstract

Apoderus dimidiatus (Coleoptera: Attelabidae), a widely distributed weevil species in China, feeds on leaves and creates compact leaf rolls for spawning. Its offspring complete a series of developmental stages within these structures before emerging as mature insects. In this study, we assembled a high-quality genome of A. dimidiatus at the chromosome level. We found the expanded gene family of A. dimidiatus is associated with functions such as the regulation of skin water loss, sebaceous gland development, and water balance in multicellular organisms, which are essential for the species’ survival within leaf rolls. On the other hand, the contracted gene family is primarily associated with protease activity and solute transmembrane transport, contributing to the decline in egg production and the low survival rate of offspring. This situation forces female adults to develop the unique behavior of leaf rolling. Overall, our findings shed light on the evolutionary relationship between A. dimidiatus and other species and elucidate the molecular mechanisms behind their unique leaf rolling behavior.

Attelabidae insects have attracted much attention due to their unique leaf rolling behavior before oviposition. However, the lack of genomic data makes it difficult to understand the molecular mechanism behind their behavior and their evolutionary relationship with other species. To address this gap, we utilized Illumina and Nanopore sequencing platforms along with Hi-C technology to establish a highly accurate whole genome of A. dimidiatus at the chromosome level. The resulting genome size was determined to be 619.26 Mb, with a contig N50 of 50.89 Mb and GC content of 33.89%. Moreover, a total of 12,572 genes were identified, with 82.59% being functionally annotated, and 64.78% designated as repeat sequences. Our subsequent phylogenetic tree analysis revealed that Attelabidae’s divergence from Curculionidae occurred approximately 161.52 million years ago. Furthermore, the genome of A. dimidiatus contained 334 expanded gene families and 1718 contracted gene families. In addition, using Phylogenetic Analysis by Maximum Likelihood (PAML), we identified 106 rapidly evolved genes exhibiting significant signals and 540 positively selected genes. Our research endeavors to serve as an invaluable genomic data resource for the study of Attelabidae, offering fresh perspectives for the exploration of its leaf rolling behavior.

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