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Schebeck, M.

Publications and source records attributed to Schebeck, M..

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Sociality in weevils is shaped by sheltering and convergent gene losses

Eusociality, characterized by overlapping generations, cooperative brood care, and reproductive division of labour, has arisen independently across diverse, phylogenetically distant insect orders, including Hymenoptera (ants, bees, and wasps), Blattodea (termites), and Coleoptera (weevils). While multiple studies have investigated the molecular evolution of sociality from solitary ancestors in Hymenoptera and Blattodea, so far little is known about the evolutionary signatures of social evolution in Coleoptera. Weevils (Curculionidae) provide an ideal system for addressing this question, as they cover the full spectrum of social complexity from parental care, through several origins of facultative eusociality to the only obligately eusocial beetle, Austroplatypus incompertus. We generated genome assemblies for A. incompertus and two facultatively eusocial weevil species, Xylosandrus germanus and Xyleborinus saxesenii, which together with 18 publicly available weevil genomes span two independent evolutionary origins of sociality. Our analyses reveal a genome-wide relaxation of purifying selection with increasing social complexity, which is most pronounced in A. incompertus. We find a significant excess of convergent gene family contractions in lineages where sociality evolved, and no evidence of elevated positive selection. These findings indicate that the molecular mechanisms of social evolution in weevils are primarily characterised by relaxed selection and gene loss, rather than adaptive innovation and gene family expansions. These observations are consistent with sheltering and reduced effective population size playing an important role, a pattern not previously observed in other clades.

evolutionary biology↗

Bark beetle protein elicitors trigger biphasic immune responses in Norway spruce seedlings

Norway spruce (Picea abies) responds to attacks by the spruce bark beetle (Ips typographus) through the rapid activation of local defense mechanisms, but field studies can be difficult to standardize due to variable attack pressure and environmental heterogeneity. Here, we developed a phytotron-based assay that mimics early beetle-associated stress using insect-derived protein extracts, enabling reproducible molecular analyses under controlled conditions. Ten-week-old spruce seedlings were stem-treated with mock buffer or beetle protein extracts, followed by transcriptomic analyses of stem tissues and targeted metabolomic profiling of needles at 2 and 48 h post-inoculation. RT-qPCR analysis revealed rapid transcriptional activation of signaling and defense genes in Norway spruce, with NP-40-based protein extracts producing the most consistent early response. RNA-seq analysis revealed transcriptional dynamics, with 488 differentially expressed genes detected at 2 h and 84 at 48 h post-inoculation relative to mock-treated controls. Early responses at 2 h were characterized by activation of genes associated with immune perception and signal transduction. By 48 h, the response shifted toward accumulation of transcripts encoding defense proteins such as chitinases, defensins, proteinase inhibitors, and pathogenesis-related (PR) proteins. Importantly, a substantial proportion of differentially expressed genes overlapped with those previously identified in mature Norway spruce trees during pioneer bark beetle attack under field conditions, supporting the biological relevance of the assay. In contrast, targeted analyses of secondary metabolites performed in needle tissue revealed limited systemic changes across time points, suggesting that early induced defenses may remain largely localized to the stem. Together, these results demonstrate that beetle-derived proteins trigger a rapid and temporally structured defense response in Norway spruce seedlings and establish a reproducible elicitor-based platform that may provide a broadly applicable framework for investigating bark beetle-induced defenses across conifers. HighlightBark beetle protein elicitors trigger temporally structured immune responses in Norway spruce seedlings that overlap with responses observed in mature trees, with rapid immune signaling at 2 h followed by defense protein accumulation at 48 h.

plant biology↗

The spruce bark beetle Ips typographus transmits mutualistic fungi in mandibular mycetangia

Insects associated with mutualistic microbes often possess structures specialized for microbial transport that ensure the maintenance of these symbioses. Called mycetangia, these structures have evolved in numerous bark beetle species facilitating fungal transport to new host trees. The Eurasian spruce bark beetle Ips typographus is associated with several filamentous ascomycetes that may provide beetles with nutrition or help overcome tree defenses. I. typographus has been believed to vector its fungal symbionts mostly on the exoskeleton, but exact mechanisms of fungal transmission are unknown. Here, we report the discovery of a mandibular mycetangium in I. typographus that enables the transmission of symbiotic fungi. Extensive fungal isolation from I. typographus heads suggested the presence of a mycetangium while micro-computed tomography and histological analyses revealed a mycetangium close to the mandibles. Strikingly, we identified these fungus-carrying structures in both sexes of I. typographus and in the congeneric species I. acuminatus, and I. duplicatus, although mandibular mycetangia have been thought to be rare in Ips bark beetles. Moreover, mycetangia in male beetles in general were hardly reported in bark beetles before. The occurrence of mycetangia in Ips species highlights the important role mutualistic fungi play in the natural history of these bark beetles.

ecology↗

Genomic Insights into the Evolution of Parental Care in Weevils

Parental care, a key step in the evolution of sociality, has evolved multiple times in insects, yet the molecular mechanisms underlying its emergence remain poorly understood. Weevils (Curculionidae) exhibit diverse parental care behaviours, from nest building to egg and larval attendance, making them an ideal system to investigate genomic changes associated with subsociality. We analysed 13 high-quality weevil genomes, encompassing independent origins of egg and larval attendance, to test two predictions: (1) the sheltering hypothesis, where parental care relaxes selection on traits critical for independent larval survival, and (2) the regulatory hypothesis, where behavioural shifts are driven by changes in transcriptional regulation. Gene family evolution analyses revealed significantly more convergent contractions, particularly in genes linked to transcriptional regulation and enzymatic activity, on branches where larval attendance evolved, consistent with functional gene loss under relaxed selection. Selection analyses identified over 400 genes under relaxed selection, especially those associated with transcriptional regulation and neural plasticity, further supporting hypothesis 1. In contrast, positive selection and intensified selection were rare but enriched for genes regulating gene expression, consistent with hypothesis 2. Together, these results suggest that parental care in weevils drives both simplification of larval traits through relaxed selection and convergent gene loss, and innovation in caregiving behaviours via adaptive changes in gene regulation. Significance statementParental care is a pivotal evolutionary innovation, yet its genetic basis in insects remains underexplored. By comparing genomes from weevil species with and without care behaviours, we reveal two key processes shaping the emergence of subsociality: relaxation of selection on genes linked to larval independence and adaptive evolution in genes regulating gene expression. This combination likely reflects reduced demands on protected larvae alongside fine-tuning of parental behaviours. Our findings highlight how simple social systems can evolve through both loss and innovation, offering a comparative framework for understanding social evolution across insects.

evolutionary biology↗

Pioneer bark beetle attacks induce multifaceted localized defense responses in Norway spruce

Conifer forests worldwide are increasingly threatened by environmental stressors, especially bark beetle infestations. In a novel experimental field setup with controlled attacks on clonal trees, we investigated the molecular defense responses of 35-year-old Norway spruce trees to colonization attempts by the spruce bark beetle, Ips typographus. A multi-omics approach was used to study tree responses to bark beetle pioneers under natural conditions. At the site of the attacks, increased levels in jasmonic acid, together with changes in other phytohormones, induced differential gene expression of up to 1,900 genes from multiple defense-related pathways. These transcriptomic alternations were corroborated by proteomic and metabolomic shifts, which ultimately showed increased levels of compounds involved in deterring bark beetle attacks, such as phenolic aglycones, diterpene resin acids, mono- and sesquiterpenes, and lignin. Our study highlights the intricate yet rapid and effective local defense response of Norway spruce against pioneer bark beetle attacks and lays a foundation for in-depth studies of this and other conifers resistance to phloem-feeding insects.

plant biology↗

Demographic history inferred from an inversion-rich spruce bark beetle genome

The demographic history of species inferred from whole-genome data provides quantitative insights into key biological parameters such as population size changes and divergence times. Reliable estimates often require data that have not been affected by selection. Extensive research, however, indicates that many species harbour multiple polymorphic chromosomal inversions, which often evolve under different selective pressures. Consequently, inversions can influence genome-wide patterns of variation and subsequent evolutionary inferences. In this study, we used genome-wide data from over 300 spruce bark beetle (Ips typographus) individuals from 23 populations across Europe to reconstruct their demographic history and to investigate the impact of a complex polymorphic inversion landscape (covering approximately 28% of the beetle genome) on demographic inference. We used two complementary methods, Pairwise Sequential Markovian Coalescent (PSMC) and Site Frequency Spectrum (SFS)-based modelling, and revealed a Late Pleistocene divergence ([~]79 kya) between populations from the southern and northern parts of the species European range, and a long-term effective population size of [~]250,000. The southern group underwent significant population expansion after this divergence event, whereas the northern group expanded during the Holocene ([~]7 kya). Recent population size estimates suggest that the southern group is twice as large as the northern group. Neglecting the presence of chromosomal inversions did not significantly affect the model selection procedure and resulted in relatively small biases in the estimated demographic parameters. This study provides information on the historical population dynamics of the spruce bark beetle and improves our understanding of the influence of a complex genomic architecture on the inference of evolutionary history.

evolutionary biology↗

Complex genomic landscape of inversion polymorphism in Europe's most destructive forest pest

In many species, polymorphic inversions underlie complex phenotypic polymorphisms and facilitate local adaptation in the face of gene flow. Multiple polymorphic inversions can co-occur in a genome, but the prevalence, evolutionary significance, and limits to complexity of genomic inversion landscapes remain poorly understood. Here, we examine genome-wide variation in one of Europes most destructive forest pests, the spruce bark beetle Ips typographus, scan for polymorphic inversions, and test whether inversions are involved in key adaptations in this species. We analyzed 240 individuals from 18 populations across the species European range and, using a whole-genome resequencing approach, identified 27 polymorphic inversions covering approximately 28% of the genome. The inversions vary in size and in levels of intra-inversion recombination, are highly polymorphic across the species range, and often overlap, forming a complex genomic architecture. We test several mechanisms, including directional selection, overdominance and associative overdominance that can contribute to the maintenance of inversion polymorphisms in the genome. We show that the heterogeneous inversion landscape is likely maintained by the combined action of several evolutionary forces and that inversions are enriched in odorant receptor genes encoding key elements of recognition pathways for host plants, mates, and symbiotic fungi. Our results indicate that the genome of this major forest pest of growing social, political, and economic importance harbors one of the most complex inversion landscapes described to date posing a question about limits of genomic architecture complexity.

evolutionary biology↗

The bacterial community of the European spruce bark beetle in space and time

The European spruce bark beetle Ips typographus is a pest causing severe damages in forests dominated by the Norway spruce in Europe. Microorganisms play an essential role in the host species performance, including nutrition, fitness as well as in overcoming host defenses. Here, we performed high-throughput 16S rRNA metabarcoding of I. typographus across different populations in Europe, to assess its bacterial community. We investigated four postglacial refugial areas in Europe and focused specifically on a current bark beetle hot spot in the Dolomites where we compared populations with different epidemiological phases (outbreaking vs. non-outbreaking) and across different seasons (pre-overwintering vs. overwintering). Our results show that the bacterial community structure varied among populations from the refugial areas and between different regions within the Dolomites. We found a significant difference in the bacterial community between pre-overwintering and overwintering individuals, but we did not find differences between epidemic and endemic populations. The prevalence of the genus Erwinia which was present in every individual and Pseudoxanthomonas in almost every individual across all populations, suggests that these taxa form the core bacterial community of I. typographus. Furthermore, several additional bacterial taxa occurred in all populations, but with variable frequencies. This study highlights a complex interaction of I. typographus and various bacterial taxa across different regions and ecological phases of I. typographus populations and provides new insights into the role of microorganisms in the biology of this important pest species.

ecology↗