Background Horizontal gene transfer (HGT) has been documented in many herbivorous insects, conferring the ability to digest plant material and promoting their remarkable ecological diversification. Previous reports suggest HGT of antibacterial enzymes may have contributed to the insect immune response and limit bacterial growth. Carnivorous insects also display many evolutionary successful lineages, but in contrast to the plant feeders, the potential role of HGTs has been less well-studied. Results Using genomic and transcriptomic data from 38 species of ladybird beetles, we identified a set of bacterial cell wall hydrolase (cwh) genes acquired by this group of beetles. Infection with Bacillus subtilis led to upregulated expression of these ladybird cwh genes, and their recombinantly produced proteins limited bacterial proliferation. Moreover, RNAi-mediated cwh knockdown led to downregulation of other antibacterial genes, indicating a role in antibacterial immune defense. cwh genes are rare in eukaryotes, but have been maintained in all tested Coccinellinae species, suggesting that this putative immune-related HGT event played a role in the evolution of this speciose subfamily of predominant predatory ladybirds. Conclusion Our work demonstrates that, in a manner analogous to HGT-facilitated plant feeding, enhanced immunity through HGT might have played a key role in the prey adaptation and niche expansion that promoted the diversification of carnivorous beetle lineages. We believe that this represents the first example of immune-related HGT in carnivorous insects with an association with a subsequent successful species radiation.

Background Members of the genus Novius Mulsant, 1846 (= Rodolia Mulsant, 1850) (Coleoptera, Coccinellidae), play important roles in the biological control of cotton cushion scale pests, especially those belonging to Icerya. Since the best-known species, the vedalia beetle Novius cardinalis (Mulsant, 1850) was introduced into California from Australia, more than a century of successful use in classical biological control, some species of Novius have begun to exhibit some field adaptations to novel but related prey species. Despite their economic importance, relatively little is known about the underlying genetic adaptations associated with their feeding habits. Knowledge of the genome sequence of Novius is a major step towards further understanding its biology and potential applications in pest control. Results We report the first high-quality genome sequence for Novius pumilus (Weise, 1892), a representative specialist of Novius. Computational Analysis of gene Family Evolution (CAFE) analysis showed that several orthogroups encoding chemosensors, digestive, and immunity-related enzymes were significantly expanded (P < 0.05) in N. pumilus compared to the published genomes of other four ladybirds. Furthermore, some of these orthogroups were under significant positive selection pressure (P < 0.05). Notably, transcriptome profiling demonstrated that many genes among the significantly expanded and positively selected orthogroups, as well as genes related to detoxification were differentially expressed, when N. pumilus feeding on the nature prey Icerya compared with the no feeding set. We speculate that these genes are vital in the Icerya adaptation of Novius species. Conclusions We report the first Novius genome thus far. In addition, we provide comprehensive transcriptomic resources for N. pumilus. The results from this study may be helpful for understanding the association of the evolution of genes related to chemosensing, digestion, detoxification and immunity with the prey adaptation of insect predators. This will provide a reference for future research and utilization of Novius in biological control programs. Moreover, understanding the possible molecular mechanisms of prey adaptation also inform mass rearing of N. pumilus and other Novius, which may benefit pest control.

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Background: Ladybird beetles (Coleoptera, Coccinellidae) are highly diverse in their feeding habits. Most of them are specialist feeders, while some can have a broad spectrum of prey. As a representative group of generalists, the tribe Coccinellini includes many aphidophagous species, but members of this tribe also feed on other hemipterous insects including coccids, psyllids and whiteflies. As a result, several species are effective biological control agents or invasive species with serious non-target effects. Despite their economic importance, relatively little is known about how they adapt to new prey. Results: In this study, comparisons of the life history traits and transcriptomes of ladybirds fed initial (aphids) and alternative prey (mealybugs) were performed in three Coccinellini species. The use of alternative prey greatly decreased performance, implied by the significantly prolonged development time and decreased survival rate and adult weight. Prey shifts resulted in a set of differentially expressed genes encoding chemosensory proteins and digestive and detoxifying enzymes. Conclusions: Our results suggest that these generalists do not perform well when they use alternative prey as the sole nutrition source. Although their capacity for predation might have created an opportunity to use varied prey, they must adapt to physiological obstacles including chemosensing, digestion and detoxification in response to a prey shift. These findings challenge the effect of Coccinellini predators on the biological control of non-aphid pests and suggest the possibility of non-target attacks by so-called specialists.

1. Bacterial symbionts can play a key role in the interactions between trophic levels. Certain symbionts are known to confer protection against natural enemies of their arthropod hosts. However, whether natural enemies evolve and adapt to prey symbionts is not well understood.2. In this study, we found that a free-living strain of aphid symbiont Serratia symbiotica, SsMj, was the most discriminative biomarker of the aphid feeding in the microbiota of aphidophagous (aphid-feeding) ladybirds. Moreover, SsMj persisted in the digestive tract of starved ladybirds and did not decay together with ingested aphid materials, suggesting horizontal transmission across trophic levels.3. We further found that SsMj did not necessarily exhibit a negative impact on aphidophagous ladybirds of the Coccinellini tribe in contrast with other, nonaphidophagous, ladybirds. First, starvation did not significantly change SsMj relative abundance or alpha microbiota diversity of an aphidophagous ladybird.Second, diets containing SsMj did not decrease the performance of the aphidophagous ladybirds. Third, infection with SsMj through injection had a minor impact on the survival of aphidophagous ladybirds.4. Together, our evidence suggests that the aphid symbiont S. symbiotica can be horizontally transmitted to ladybird predators. At the same time, the group of ladybirds that have adapted to feeding on aphids have also evolved to establish a nearly neutral relationship with S. symbiotica, suggesting adaptation to a prey symbiont.