Martin Kaltenpoth

Many herbivorous beetles depend on plant cell wall-degrading enzymes (PCWDEs) to access the nutritious plant cell content. However, the evolution of PCWDEs in weevils, the most diverse lineage of herbivores, remains poorly understood. Using transcriptomic and genomic analyses of 45 weevil species spanning the majority of existing subfamilies, we identified a total of 13 different PCWDE families, revealing high variability between species. Interestingly, the PCWDE repertoires tracked dietary specialization, with convergent reductions in fungivorous taxa. Furthermore, PCWDE gene family dynamics were driven by both larval and adult specialized herbivory on different plant organs. Despite this complex evolutionary history, phylogenetic analyses place core PCWDE functionalities at the base of the Phytophaga (weevils, leaf beetles, and longhorn beetles) and reveal subsequent horizontal gene transfer (HGT) events from various donors during early Phytophaga diversification. These findings demonstrate that HGTs, gene duplications, and losses shaped PCWDE diversity and facilitated the ecological success of weevils.

Nutritional symbioses have repeatedly evolved in insects, yet how hosts regulate these partnerships to balance benefits across development and environments remains unclear. Ants provide an exceptional system to address this question, as several lineages maintain ancient symbionts that can be naturally lost without harming the host. The invasive tramp ant Cardiocondyla obscurior provides a compelling example of this phenomenon, as the vertically transmitted symbiont Candidatus Westeberhardia cardiocondylae can be lost at the species, colony, and even individual level. By implementing a range of molecular techniques, including dual-RNA sequencing, fluorescent in-situ hybridisations of RNA and qPCR, in conjunction with experimental manipulations of diet, we reveal the regulatory dynamics and function of this labile association. Symbionts provide shikimate-derived nutrients that enhance colony resilience under protein limitation, while hosts appear to regulate symbiont abundance during protein scarcity and cuticle formation to optimise resource allocation. In the symbiont’s absence, ants compensate by upregulating genes enabling tyrosine acquisition from external sources. This metabolic flexibility allows colonies to exploit symbiont-derived and environmental nutrients, sustaining both growth and survival across nutritional contexts. Our findings reveal dynamic host regulation as a mechanism for sustaining the persistence and adaptability of ancient symbioses.

Animals are not known to biosynthesize floral chemical signals to manipulate pollinators, although such mimicry could profoundly shape plant–pollinator interactions. Larvae of the poisonous European blister beetle Meloe proscarabaeus parasitize multiple solitary bee species, yet the mechanism enabling host attraction has remained unresolved. Here we show that these larvae lure bees by emitting a bouquet of volatile compounds that closely resembles floral scent. Chemical analyses reveal a complex blend of monoterpenoids derived from ( S )-linalool, a ubiquitous floral volatile. Behavioral assays demonstrate that these compounds function as floral-scent mimics, eliciting attraction in bees and acting as allomones (i.e., interspecific chemical signals that benefit the emitter while disadvantaging the receiver). Transcriptomic and functional analyses identify cytochrome P450 enzymes that oxidize ( S )-linalool, suggesting that larvae biosynthesize these plant-like volatiles de novo. Together, these findings broaden the scope of interkingdom chemical mimicry and uncover a striking form of sensory deception in which an insect chemically assumes the signal identity of a flower, revealing that animals can evolve biosynthetic pathways to exploit plant–pollinator communication.

The Eurasian spruce bark beetle Ips typographus , a major forest pest on Norway spruce ( Picea abies ), forms intimate associations with several types of microbial symbionts. While previous research has focused primarily on filamentous fungi, yeasts have remained largely unexplored. Here, we show that yeasts associated with I. typographus may contribute to host tree colonization by providing defensive benefits. Dominant yeasts ( Yamadazyma , Kuraishia , Nakazawaea, and Wickerhamomyces ), which are phylogenetically related to other insect-associated Saccharomycotina, significantly attract adult beetles. Moreover, several yeasts inhibit the growth of the pathogenic fungus Trichoderma harzianum in vitro , and beetle eggs benefit from the presence of Kuraishia capsulata by reduced fungal infection under semi-natural conditions. Strikingly, these effects are mediated by the yeasts’ transformation of the tree’s defensive stilbene glycosides into antimicrobial aglycones and phenolic acids that accumulate in beetle galleries. These findings reveal a previously unrecognized role of symbiotic yeasts in converting spruce defensive stilbene glycosides into antimicrobial aglycones and oxidative cleavage products that accumulate in beetle galleries, and might contribute to the survival of their bark beetle host.

With over a million described species, insects represent the most successful group of animals on Earth. One of the drivers of insect diversity is their ability to engage in multifold beneficial symbioses with microorganisms, often involving specialized host organs to accommodate intra- or extracellular symbionts. The existence of such organs and their importance for sustaining and transmitting beneficial symbionts has been known for over a century, and specific terms have been established for categorizing organs harbouring intracellular bacteria (bacteriomes) or fungi (mycetomes), or cuticular crypts containing extracellular fungi (mycetangia). For others, however, general terms are lacking, e.g. organs containing extracellular bacteria associated with the cuticle or with the digestive tract. Furthermore, previously established terms have been misused in other contexts. Notably, ‘bacteriome’ has been increasingly employed in the microbiome field to refer to bacterial communities, instead of the term’s original meaning of specialized organs housing intracellular bacterial symbionts. Here, we review and categorize the diversity of symbiotic organs in insects and propose a unified terminology. Our hope is that this common language will facilitate communication and thereby support the field of symbiosis research in unravelling commonalities and differences in the evolution, ecology, development, physiology and molecular basis across symbiotic interactions. This article is part of the theme issue ‘Life in natural microcosms’.

With advances in imaging technologies and the growing availability of specialized lights and cameras, biofluorescence is increasingly recognized as a widespread trait with potential roles in the behavioural ecology of many tetrapods. Here, we report the first evidence of biofluorescence in the fire salamander (Salamandra salamandra), one of Europe’s most studied amphibians. Under UV illumination, S. salamandra exhibited conspicuous external fluorescence, mainly on the ventral and lateral surfaces and in glandular secretions. Histological analyses revealed that UV–violet excitation produces a broad blue–green fluorescence in the epidermis and granular glands, matching the emission of secretions and the speckled external pattern corresponding to glandular ducts. Fluorescence lifetime imaging revealed that glandular fluorophores differ from those in the epidermis and are also ubiquitous in blood components, suggesting that fluorescent compounds may be transported via the circulatory system, a feature previously known only in tree frogs. Additionally, a secondary yellow fluorescence was detected in the dermal chromatophore layer, excited exclusively by UV light. Notably, fluorescence from secretions persisted on substrates for over 24 h and fulfilled several criteria for ecological relevance, suggesting a communicative function for this trait and adding to the growing evidence of ecologically relevant fluorescence in amphibians.

Genetic variation contributes to intraspecific differences in the chemical defence in many insect species, yet the underlying genetic mechanisms remain poorly understood. The horseradish flea beetle, Phyllotreta armoraciae , sequesters glucosinolates from its horseradish host plant and activates them using endogenous myrosinase enzymes. Of the three known myrosinases in P. armoraciae , PaMyr1 functions primarily in adults, whereas PaMyr2 and PaMyr3 are responsible for myrosinase activity in larvae. Here, we identify natural genetic variation at the myrosinase locus that gives rise to three distinct myrosinase haplotypes, only one of which retains a functional PaMyr3 gene. This variation affected PaMyr gene expression and myrosinase activity in larvae but not in adults. Larvae expressing both PaMyr2 and PaMyr3 showed elevated myrosinase activity toward 2‐propenyl glucosinolate, the major glucosinolate in horseradish. Gene expression and biochemical analyses indicate that elevated myrosinase activity results from a subfunctionalization of PaMyr3, which confers greater catalytic efficiency rather than higher total myrosinase abundance. Importantly, PaMyr3 ‐expressing larvae were less susceptible to a model generalist predator in laboratory assays, suggesting a selective advantage under high predation pressure. Consistent with this hypothesis, the PaMyr3 ‐containing haplotype occurred at higher frequency in a natural population than in long‐term laboratory populations lacking predators. Together, our results link structural genetic variation to intraspecific differences in insect chemical defence with potential consequences for predator–prey interactions in natural populations.

Animals encounter diverse ecological factors that shape their microbiota. While plants often provide nutrition, some animals also utilise them for non‐nutritional purposes, that is, pharmacophagy. Although both uses may influence herbivore microbiomes, the effects of pharmacophagy remain underexplored. We studied such effects in the holometabolous insect Athalia rosae , whose larvae feed on Brassicaceae plants, while adults take up nectar from Apiaceae and, additionally, clerodanoids (plant specialised metabolites) through pharmacophagy from Lamiaceae species. We examined how nutritional and non‐nutritional plant use affect microbiota diversity, composition and predicted function. We also tested whether the microbiota of larval faeces can serve as a non‐invasive proxy for larval microbiota and compared microbiota profiles across rearing environments (laboratory vs. wild) and specific life stages (i.e., larvae vs. adults). Microbiota composition was highly context‐dependent, with indicator species analyses revealing treatment‐specific amplicon sequence variants. Diet, starvation and clerodanoid access each resulted in distinct communities; faeces reliably reflected larval microbiota; and wild‐caught adults harboured the most diverse communities. Predicted microbial functions varied with diet and pharmacophagy, particularly in pathways putatively linked to metabolite degradation, energy metabolism and detoxification. Together, our findings suggest that both nutritional and non‐nutritional plant use shape intraspecific microbiota variation in insects.