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Complex Genomic Landscape of Inversion Polymorphism in Europe’s Most Destructive Forest Pest

Mykhailenko, Anastasiia ; Zieliński, Piotr ; Bednarz, Aleksandra ; Schlyter, Fredrik ; Andersson, Martin N. LU ; Antunes, Bernardo ; Borowski, Zbigniew ; Krokene, Paal ; Melin, Markus and Morales-García, Julia , et al. (2024) In Genome Biology and Evolution 16(12).
Abstract

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... (More)

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.

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type
Contribution to journal
publication status
published
subject
keywords
forest pest, genome complexity, Ips typographus, polymorphic inversions, spruce bark beetle
in
Genome Biology and Evolution
volume
16
issue
12
article number
evae263
publisher
Oxford University Press
external identifiers
  • pmid:39656753
  • scopus:85212825920
ISSN
1759-6653
DOI
10.1093/gbe/evae263
language
English
LU publication?
yes
id
ace69576-090e-4716-8b8c-db3d50525112
date added to LUP
2025-01-17 14:14:41
date last changed
2025-07-05 04:38:12
@article{ace69576-090e-4716-8b8c-db3d50525112,
  abstract     = {{<p>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.</p>}},
  author       = {{Mykhailenko, Anastasiia and Zieliński, Piotr and Bednarz, Aleksandra and Schlyter, Fredrik and Andersson, Martin N. and Antunes, Bernardo and Borowski, Zbigniew and Krokene, Paal and Melin, Markus and Morales-García, Julia and Müller, Jörg and Nowak, Zuzanna and Schebeck, Martin and Stauffer, Christian and Viiri, Heli and Zaborowska, Julia and Babik, Wiesław and Nadachowska-Brzyska, Krystyna}},
  issn         = {{1759-6653}},
  keywords     = {{forest pest; genome complexity; Ips typographus; polymorphic inversions; spruce bark beetle}},
  language     = {{eng}},
  number       = {{12}},
  publisher    = {{Oxford University Press}},
  series       = {{Genome Biology and Evolution}},
  title        = {{Complex Genomic Landscape of Inversion Polymorphism in Europe’s Most Destructive Forest Pest}},
  url          = {{http://dx.doi.org/10.1093/gbe/evae263}},
  doi          = {{10.1093/gbe/evae263}},
  volume       = {{16}},
  year         = {{2024}},
}