Highly transmissible cytoplasmic incompatibility by the extracellular insect symbiont Spiroplasma.

Cytoplasmic incompatibility (CI) is a form of reproductive manipulation caused by maternally inherited endosymbionts infecting arthropods, like Wolbachia, whereby matings between infected males and uninfected females produce few or no offspring. We report the discovery of a new CI symbiont, a strain of Spiroplasma causing CI in the parasitoid wasp Lariophagus distinguendus. Its extracellular occurrence enabled us to establish CI in uninfected adult insects by transferring Spiroplasma-infected hemolymph. We sequenced the CI-Spiroplasma genome and did not find any homologues of any of the cif genes discovered to cause CI in Wolbachia, suggesting independent evolution of CI. Instead, the genome contains other potential CI-causing candidate genes, such as homologues of high-mobility group (HMG) box proteins that are crucial in eukaryotic development but rare in bacterial genomes. Spiroplasma's extracellular nature and broad host range encompassing medically and agriculturally important arthropods make it a promising tool to study CI and its applications.

A multitaxa assessment of the effectiveness of agri-environmental schemes for biodiversity management.

Agri-environmental schemes (AES) aim to restore biodiversity and biodiversity-mediated ecosystem services in landscapes impoverished by modern agriculture. However, a systematic, empirical evaluation of different AES types across multiple taxa and functional groups is missing. Within one orthogonal design, we studied sown flowering AES types with different temporal continuity, size, and landscape context and used calcareous grasslands as seminatural reference habitat. We measured species richness of 12 taxonomic groups (vascular plants, cicadas, orthopterans, bees, butterflies, moths, hoverflies, flower visiting beetles, parasitoid wasps, carabid beetles, staphylinid beetles, and birds) representing 5 trophic levels. A total of 54,955 specimens were identified using traditional taxonomic methods, and bulk arthropod samples were identified through DNA metabarcoding, resulting in a total of 1,077 and 2,110 taxa, respectively. Species richness of most taxonomic groups, as well as multidiversity and richness of pollinators, increased with temporal continuity of AES types. Some groups responded to size and landscape context, but multidiversity and richness of pollinators and natural enemies were not affected. AES flowering fields supported different species assemblages than calcareous grasslands, but assemblages became more similar to those in seminatural grasslands with increasing temporal continuity. Our results indicate that AES flowering fields and seminatural grasslands function synergistically. Flowering fields support biodiversity even when they are relatively small and in landscapes with few remaining seminatural habitats. We therefore recommend a network of smaller, temporally continuous AES flowering fields of different ages, combined with permanent seminatural grasslands, to maximize benefits for biodiversity conservation and ecosystem service delivery in agricultural landscapes.

Reproductive isolation due to prezygotic isolation and postzygotic cytoplasmic incompatibility in parasitoid wasps.

The reproductive barriers that prevent gene flow between closely related species are a major topic in evolutionary research. Insect clades with parasitoid lifestyle are among the most species-rich insects and new species are constantly described, indicating that speciation occurs frequently in this group. However, there are only very few studies on speciation in parasitoids. We studied reproductive barriers in two lineages of Lariophagus distinguendus (Chalcidoidea: Hymenoptera), a parasitoid wasp of pest beetle larvae that occur in human environments. One of the two lineages occurs in households preferably attacking larvae of the drugstore beetle Stegobium paniceum ("DB-lineage"), the other in grain stores with larvae of the granary weevil Sitophilus granarius as main host ("GW-lineage"). Between two populations of the DB-lineage, we identified slight sexual isolation as intraspecific barrier. Between populations from both lineages, we found almost complete sexual isolation caused by female mate choice, and postzygotic isolation, which is partially caused by cytoplasmic incompatibility induced by so far undescribed endosymbionts which are not Wolbachia or Cardinium. Because separation between the two lineages is almost complete, they should be considered as separate species according to the biological species concept. This demonstrates that cryptic species within parasitoid Hymenoptera also occur in Central Europe in close contact to humans.

Does early learning drive ecological divergence during speciation processes in parasitoid wasps?

Central to the concept of ecological speciation is the evolution of ecotypes, i.e. groups of individuals occupying different ecological niches. However, the mechanisms behind the first step of separation, the switch of individuals into new niches, are unclear. One long-standing hypothesis, which was proposed for insects but never tested, is that early learning causes new ecological preferences, leading to a switch into a new niche within one generation. Here, we show that a host switch occurred within a parasitoid wasp, which is associated with the ability for early learning and the splitting into separate lineages during speciation. Lariophagus distinguendus consists of two genetically distinct lineages, most likely representing different species. One attacks drugstore beetle larvae (Stegobium paniceum (L.)), which were probably the ancestral host of both lineages. The drugstore beetle lineage has an innate host preference that cannot be altered by experience. In contrast, the second lineage is found on Sitophilus weevils as hosts and changes its preference by early learning. We conclude that a host switch has occurred in the ancestor of the second lineage, which must have been enabled by early learning. Because early learning is widespread in insects, it might have facilitated ecological divergence and associated speciation in this hyperdiverse group.