Molecular evolution of dietary shifts in ladybird beetles (Coleoptera: Coccinellidae): from fungivory to carnivory and herbivory

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BACKGROUND: Dietary shifts are major evolutionary steps that shape ecological niches and biodiversity. The beetle family Coccinellidae, commonly known as ladybirds, first transitioned from a fungivorous to an insectivorous and subsequently a plant diet. However, the molecular basis of this dietary diversification remained unexplored. RESULTS: We investigated the molecular evolution of dietary shifts in ladybirds, focusing on the transitions from fungivory to carnivory (Coccinellidae) and from carnivory to herbivory (Epilachnini), by comparing 25 genomes and 62 transcriptomes of beetles. Our analysis shows that chemosensory gene families have undergone significant expansions at both nodes of diet change and were differentially expressed in feeding experiments, suggesting that they may be related to foraging. We found expansions of digestive and detoxifying gene families and losses of chitin-related digestive genes in the herbivorous ladybirds, and absence of most plant cell wall-degrading enzymes in the ladybirds dating from the transition to carnivory, likely indicating the effect of different digestion requirements on the gene repertoire. Immunity effector genes tend to emerge or have specific amino acid sequence compositions in carnivorous ladybirds and are downregulated under suboptimal dietary treatments, suggesting a potential function of these genes related to microbial symbionts in the sternorrhynchan prey. CONCLUSIONS: Our study provides a comprehensive comparative genomic analysis to address evolution of chemosensory, digestive, detoxifying, and immune genes associated with dietary shifts in ladybirds. Ladybirds can be considered a ubiquitous example of dietary shifts in insects, and thus a promising model system for evolutionary and applied biology.

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