In many species, polymorphic genomic 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 genetic variation in one of Europe's most destructive forest pests, the spruce bark beetle Ips typographus, scan for polymorphic inversions, and test whether inversions are associated with key traits 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 ∼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 found no support for mechanisms such as directional selection, overdominance, and associative overdominance that are often invoked to explain the presence of large inversion polymorphisms in the genome. This suggests that inversions are either neutral or maintained by the combined action of multiple evolutionary forces. We also found that inversions are enriched in odorant receptor genes encoding 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 and raise questions about the limits of intraspecific genomic architecture complexity.

Bavarian Forest National Park 94481 Grafenau Germany

Chemical Ecology Department of Plant Protection Biology Swedish University of Agricultural Sciences Alnarp 234 22 Lomma Sweden

Departament of Forest Ecology Forest Research Institute 05 090 Raszyn Poland

Department of Biology Lund University 223 62 Lund Sweden

Division of Biotechnology and Plant Health Norwegian Institute of Bioeconomy Research 1433 Ås Norway

Doctoral School of Exact and Natural Sciences Jagiellonian University 30 348 Kraków Poland

ETM Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague 165 00 Praha Czechia

Field Station Fabrikschleichach Animal Ecology and Tropical Biology Biocenter University of Würzburg 96181 Rauhenebrach Germany

Forest Health and Bidiversity Group Natural Resources Institute Finland 80100 Joensuu Finland

Institute of Environmental Sciences Faculty of Biology Jagiellonian University 30 387 Kraków Poland

Institute of Forest Entomology Forest Pathology and Forest Protection Department of Forest and Soil Sciences University of Natural Resources and Life Sciences Vienna 1190 Vienna Austria

UPM Forest UPM Kymmene 33100 Tampere Finland

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