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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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 |
work_keys_str_mv |
AT zoranakurbalijanovicic negativefrequencydependentselectioncontributestothemaintenanceofaglobalpolymorphisminmitochondrialdna AT ahmedsayadi negativefrequencydependentselectioncontributestothemaintenanceofaglobalpolymorphisminmitochondrialdna AT mihailojelic negativefrequencydependentselectioncontributestothemaintenanceofaglobalpolymorphisminmitochondrialdna AT goranarnqvist negativefrequencydependentselectioncontributestothemaintenanceofaglobalpolymorphisminmitochondrialdna |
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