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Description
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The megadiverse Phytophaga (leaf beetles, longhorned beetles and weevils) rely on a suite of digestive enzymes to break down plant cell wall (PCW) polysaccharides, which allowed them to diversify on an herbivorous diet. While the evolutionary histories of PCW-degrading enzymes (PCWDEs) have been characterized on the subfamily level for leaf beetles and longhorned beetles, the knowledge remains fragmentary for weevils, the taxonomically and ecologically most diverse of the three taxa. Using transcriptomic and genomic data, we characterized the PCWDE-encoding genes across 45 weevil species, representing the majority of extant subfamilies. We report the presence of 13 PCWDE families (1-9 per species), including the first description of putative endo-α-1,5-L-arabinanases in animals. Interestingly, we found strong evidence that PCWDE gene family dynamics were driven by both larval and adult dietary specialization. In particular, reduced sets of PCWDEs coincided with convergent dietary shifts towards fungivory. Phylogenetic analyses of PCWDE families across Phytophaga revealed the likely sequence of horizontal gene transfers (HGTs) along the Phytophaga stem- to crown-group radiation. Surprisingly, not only cellulase and pectinase, but also hemicellulase activity was predicted for the Phytophaga ancestor due to ancient HGT events, likely facilitating the shift towards an herbivorous diet. Our study provides novel insights into the diversity and evolution of PCWDEs within weevils, reinforcing the important role of HGTs, gene duplications, and gene losses in the evolution of the enzymatic machineries for PCW degradation, a key factor contributing to one of the most successful adaptive radiations on the planet.
Supplementary data 2 (files Supporting_data_1A.zip and Supporting_Data_1B.fasta) contains the draft genome assembly (unpolished (1A) and polished with final error correction (1B)) of the beetle A. fasciculatus.
Supplementary data 3 (file Supporting_data_2.zip) contains the codon-based nucleotide alignment (FASTA file), the IQ-TREE log file and the resulting tree file (Newick file) used to generate Fig. 1.
Supplementary data 4 (file Supporting_data_3_updated.zip) contains the amino acid alignments (FASTA file) and the resulting tree files (Newick format) of all the phylogenetic analyses of PCWDE families presented in the paper.
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Keyword
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weevils, Curculionoidea, horizontal gene transfer, herbivory, plant cell wall- degrading enzymes, cellulase, pectinase, dietary shift |
