Negative frequency dependent selection contributes to the maintenance of a global polymorphism in mitochondrial DNA

Abstract Background Understanding the forces that maintain diversity across a range of scales is at the very heart of biology. Frequency-dependent processes are generally recognized as the most central process for the maintenance of ecological diversity. The same is, however, not generally true for...

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Main Authors: Zorana Kurbalija Novičić, Ahmed Sayadi, Mihailo Jelić, Göran Arnqvist
Format: Article
Language:English
Published: BMC 2020-02-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:https://doi.org/10.1186/s12862-020-1581-2
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spelling doaj-b93ac5e699d4449fb2d2f8ab45cb7dfb2021-09-02T20:20:03ZengBMCBMC Evolutionary Biology1471-21482020-02-012011910.1186/s12862-020-1581-2Negative frequency dependent selection contributes to the maintenance of a global polymorphism in mitochondrial DNAZorana Kurbalija Novičić0Ahmed Sayadi1Mihailo Jelić2Göran Arnqvist3Animal Ecology, Department of Ecology and Genetics, Evolutionary Biology Center, Uppsala UniversityAnimal Ecology, Department of Ecology and Genetics, Evolutionary Biology Center, Uppsala UniversityFaculty of Biology, University of BelgradeAnimal Ecology, Department of Ecology and Genetics, Evolutionary Biology Center, Uppsala UniversityAbstract Background Understanding the forces that maintain diversity across a range of scales is at the very heart of biology. Frequency-dependent processes are generally recognized as the most central process for the maintenance of ecological diversity. The same is, however, not generally true for genetic diversity. Negative frequency dependent selection, where rare genotypes have an advantage, is often regarded as a relatively weak force in maintaining genetic variation in life history traits because recombination disassociates alleles across many genes. Yet, many regions of the genome show low rates of recombination and genetic variation in such regions (i.e., supergenes) may in theory be upheld by frequency dependent selection. Results We studied what is essentially a ubiquitous life history supergene (i.e., mitochondrial DNA) in the fruit fly Drosophila subobscura, showing sympatric polymorphism with two main mtDNA genotypes co-occurring in populations world-wide. Using an experimental evolution approach involving manipulations of genotype starting frequencies, we show that negative frequency dependent selection indeed acts to maintain genetic variation in this region. Moreover, the strength of selection was affected by food resource conditions. Conclusions Our work provides novel experimental support for the view that balancing selection through negative frequency dependency acts to maintain genetic variation in life history genes. We suggest that the emergence of negative frequency dependent selection on mtDNA is symptomatic of the fundamental link between ecological processes related to resource use and the maintenance of genetic variation.https://doi.org/10.1186/s12862-020-1581-2Balancing selectionMitochondriamtDNAPolymorphismNegative frequency dependent selection
collection DOAJ
language English
format Article
sources DOAJ
author Zorana Kurbalija Novičić
Ahmed Sayadi
Mihailo Jelić
Göran Arnqvist
spellingShingle Zorana Kurbalija Novičić
Ahmed Sayadi
Mihailo Jelić
Göran Arnqvist
Negative frequency dependent selection contributes to the maintenance of a global polymorphism in mitochondrial DNA
BMC Evolutionary Biology
Balancing selection
Mitochondria
mtDNA
Polymorphism
Negative frequency dependent selection
author_facet Zorana Kurbalija Novičić
Ahmed Sayadi
Mihailo Jelić
Göran Arnqvist
author_sort Zorana Kurbalija Novičić
title Negative frequency dependent selection contributes to the maintenance of a global polymorphism in mitochondrial DNA
title_short Negative frequency dependent selection contributes to the maintenance of a global polymorphism in mitochondrial DNA
title_full Negative frequency dependent selection contributes to the maintenance of a global polymorphism in mitochondrial DNA
title_fullStr Negative frequency dependent selection contributes to the maintenance of a global polymorphism in mitochondrial DNA
title_full_unstemmed Negative frequency dependent selection contributes to the maintenance of a global polymorphism in mitochondrial DNA
title_sort negative frequency dependent selection contributes to the maintenance of a global polymorphism in mitochondrial dna
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2020-02-01
description Abstract Background Understanding the forces that maintain diversity across a range of scales is at the very heart of biology. Frequency-dependent processes are generally recognized as the most central process for the maintenance of ecological diversity. The same is, however, not generally true for genetic diversity. Negative frequency dependent selection, where rare genotypes have an advantage, is often regarded as a relatively weak force in maintaining genetic variation in life history traits because recombination disassociates alleles across many genes. Yet, many regions of the genome show low rates of recombination and genetic variation in such regions (i.e., supergenes) may in theory be upheld by frequency dependent selection. Results We studied what is essentially a ubiquitous life history supergene (i.e., mitochondrial DNA) in the fruit fly Drosophila subobscura, showing sympatric polymorphism with two main mtDNA genotypes co-occurring in populations world-wide. Using an experimental evolution approach involving manipulations of genotype starting frequencies, we show that negative frequency dependent selection indeed acts to maintain genetic variation in this region. Moreover, the strength of selection was affected by food resource conditions. Conclusions Our work provides novel experimental support for the view that balancing selection through negative frequency dependency acts to maintain genetic variation in life history genes. We suggest that the emergence of negative frequency dependent selection on mtDNA is symptomatic of the fundamental link between ecological processes related to resource use and the maintenance of genetic variation.
topic Balancing selection
Mitochondria
mtDNA
Polymorphism
Negative frequency dependent selection
url https://doi.org/10.1186/s12862-020-1581-2
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AT ahmedsayadi negativefrequencydependentselectioncontributestothemaintenanceofaglobalpolymorphisminmitochondrialdna
AT mihailojelic negativefrequencydependentselectioncontributestothemaintenanceofaglobalpolymorphisminmitochondrialdna
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