A common venomous ancestor? Prevalent bee venom genes evolved before the aculeate stinger while few major toxins are bee-specific

Abstract

Venoms have convergently evolved in all major animal lineages and are ideal candidates to unravel the genomic processes underlying convergent trait evolution. However, few animal groups have been studied in detail, and large-scale comparative genomic analyses to address toxin gene evolution are rare. The hyper-diverse hymenopterans are the most speciose group of venomous animals, but the origin of their toxin genes has been largely overlooked. We combined proteo-transcriptomics with comparative genomics compiling an up-to-date list of core bee venom proteins to investigate the origin of 11 venom genes in 30 hymenopteran genomes including two newly sequenced genomes of stingless bees. We found a more distinct pattern in which toxin genes originated predominantly by single gene co-option, a prevalent mechanism in parasitoid wasps. These are always accompanied by parallel expansion events in other bee and hymenopteran sister gene groups. The short toxic peptides melittin and apamin appear to be unique to bees, a result supported by a novel machine learning approach. Based on the syntenic pattern we propose here Anthophilin1 as a bee-unique gene family that includes apamin and MCDP. It appears that bees co-adapted their venom genes which predominantly already existed before the aculeate ovipositor evolved to a stinger which exclusively injects venom. Our results provide insight into the large-scale evolution of bee venom compounds, and we present here the first study revealing general processes of venom evolution at a comparative genomic level for this mega-diverse Hymenoptera.

The Pharmacological Potential of Novel Melittin Variants from the Honeybee and Solitary Bees against Inflammation and Cancer

“…For more details on available melittin peptides and the processing and availability of the novel proteo-transcriptome data, please see BioProject (PRJNA733472), von Reumont, et al [5], and Koludarov et al [7].…”

“…Besides this important function, hymenopterans are also the animal group that harbors the most venomous species. In particular, the aculeates (bees, wasps, and ants) that evolved the characteristic waist in combination with the stinger as a modified ovipositor that is solely used for predation or defense are notoriously recognized to employ venom [7,8]. Since aculeates and especially honeybees (Apis spp.)…”

“…Only a small subset of species has been studied, and few analyses have been conducted focusing on solitary bee species to identify and test anti-microbial peptides. Recently, the venoms of the solitary bees Xylocopa violacea and Halictus scabiosae (and complementary Apis mellifera) were proteo-transcriptomically analyzed in combination with comparative genomics to unravel the evolution of prevalent bee venom genes [7,19]. Interestingly, most of the small peptides identified in the solitary bees such as halictin (Hal), codesane (Cod), xylopin (Xac), melectin (Mel), and osmin (Osm) were identified as variants of melittin, which is a toxin family unique to bees sensu lato [7].…”

“…Recently, the venoms of the solitary bees Xylocopa violacea and Halictus scabiosae (and complementary Apis mellifera) were proteo-transcriptomically analyzed in combination with comparative genomics to unravel the evolution of prevalent bee venom genes [7,19]. Interestingly, most of the small peptides identified in the solitary bees such as halictin (Hal), codesane (Cod), xylopin (Xac), melectin (Mel), and osmin (Osm) were identified as variants of melittin, which is a toxin family unique to bees sensu lato [7]. However, the bioactivity of these peptides and thus their pharmacological potential has not yet been elucidated.…”

Behavioural Indicators of Pain and Suffering in Arthropods and Might Pain Bite Back?

“…However, bees evolved a non-predatory life from wasp ancestors but retained the sting [ 94 ]. Here, the sting is often used to deter potential predators, particularly important in social species, and these venoms cause pain in mammals [ 93 , 95 ]. They also use stings, however, in defence against other invertebrates and in intraspecific contests.…”