How chromosomal inversions reorient the evolutionary process

Author:

Berdan Emma L.12ORCID,Barton Nicholas H.3ORCID,Butlin Roger41ORCID,Charlesworth Brian5ORCID,Faria Rui67ORCID,Fragata Inês8ORCID,Gilbert Kimberly J.9ORCID,Jay Paul10ORCID,Kapun Martin1112ORCID,Lotterhos Katie E.13ORCID,Mérot Claire14ORCID,Durmaz Mitchell Esra159ORCID,Pascual Marta16ORCID,Peichel Catherine L.17ORCID,Rafajlović Marina181ORCID,Westram Anja M.193ORCID,Schaeffer Stephen W.20ORCID,Johannesson Kerstin2118ORCID,Flatt Thomas9ORCID

Affiliation:

1. Department of Marine Sciences University of Gothenburg Gothenburg Sweden

2. Bioinformatics Core, Department of Biostatistics Harvard T. H. Chan School of Public Health Boston Massachusetts USA

3. Institute of Science and Technology Austria (ISTA) Klosterneuburg Austria

4. Ecology and Evolutionary Biology, School of Bioscience The University of Sheffield Sheffield UK

5. Institute of Ecology and Evolution, School of Biological Sciences University of Edinburgh Edinburgh UK

6. BIOPOLIS Program in Genomics Biodiversity and Land Planning, CIBIO Vairão Portugal

7. CIBIO-InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos Universidade do Porto Vairão Portugal

8. CHANGE - Global Change and Sustainability Institute/Animal Biology Department, cE3c - Center for Ecology, Evolution and Environmental Changes, Faculty of Sciences University of Lisbon Lisbon Portugal

9. Department of Biology University of Fribourg Fribourg Switzerland

10. Center for GeoGenetics University of Copenhagen Copenhagen Denmark

11. Central Research Laboratories Natural History Museum of Vienna Vienna Austria

12. Center for Anatomy and Cell Biology Medical University of Vienna Vienna Austria

13. Department of Marine and Environmental Sciences Northeastern University Boston Massachusetts USA

14. UMR 6553 Ecobio, Université de Rennes, OSUR, CNRS Rennes France

15. Functional Genomics & Metabolism Research Unit, Department of Biochemistry and Molecular Biology University of Southern Denmark Odense M Denmark

16. Departament de Genètica, Microbiologia i Estadística Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona Barcelona Spain

17. Division of Evolutionary Ecology, Institute of Ecology and Evolution University of Bern Bern Switzerland

18. Linnaeus Centre for Marine Evolutionary Biology University of Gothenburg Gothenburg Sweden

19. Faculty of Biosciences and Aquaculture Nord University Bodø Norway

20. Department of Biology Pennsylvania State University University Park Pennsylvania USA

21. Tjärnö Marine Laboratory, Department of Marine Sciences University of Gothenburg Strömstad Sweden

Abstract

Abstract Inversions are structural mutations that reverse the sequence of a chromosome segment and reduce the effective rate of recombination in the heterozygous state. They play a major role in adaptation, as well as in other evolutionary processes such as speciation. Although inversions have been studied since the 1920s, they remain difficult to investigate because the reduced recombination conferred by them strengthens the effects of drift and hitchhiking, which in turn can obscure signatures of selection. Nonetheless, numerous inversions have been found to be under selection. Given recent advances in population genetic theory and empirical study, here we review how different mechanisms of selection affect the evolution of inversions. A key difference between inversions and other mutations, such as single nucleotide variants, is that the fitness of an inversion may be affected by a larger number of frequently interacting processes. This considerably complicates the analysis of the causes underlying the evolution of inversions. We discuss the extent to which these mechanisms can be disentangled, and by which approach. Abstract Inversions often play key roles in adaptation and speciation, but the processes that direct their evolution are obscured by the characteristic that makes them so unique (reduced recombination between arrangements). In this review, we examine how different mechanisms can impact inversion evolution, weaving together both theoretical and empirical studies. We emphasize that most patterns are overdetermined (i.e. can be caused by multiple processes), but we highlight new technologies that provide a path forward towards disentangling these mechanisms.

Funder

Directorate for Biological Sciences

European Commission

European Society for Evolutionary Biology

Fundação para a Ciência e a Tecnologia

Leverhulme Trust

Norges Forskningsråd

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

Vetenskapsrådet

Publisher

Oxford University Press (OUP)

Subject

Ecology, Evolution, Behavior and Systematics

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