The potential of inversions to accumulate balanced sexual antagonism is supported by simulations and Drosophila experiments
Chromosomal inversion polymorphisms can be common, but the causes of their persistence are often unclear. We propose a model for the maintenance of inversion polymorphism, which requires that some variants contribute antagonistically to two phenotypes, one of which has negative frequency-dependent f...
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eLife Sciences Publications Ltd
2025-04-01
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| author | Christopher S McAllester John E Pool |
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| description | Chromosomal inversion polymorphisms can be common, but the causes of their persistence are often unclear. We propose a model for the maintenance of inversion polymorphism, which requires that some variants contribute antagonistically to two phenotypes, one of which has negative frequency-dependent fitness. These conditions yield a form of frequency-dependent disruptive selection, favoring two predominant haplotypes segregating alleles that favor opposing antagonistic phenotypes. An inversion associated with one haplotype can reduce the fitness load incurred by generating recombinant offspring, reinforcing its linkage to the haplotype and enabling both haplotypes to accumulate more antagonistic variants than expected otherwise. We develop and apply a forward simulator to examine these dynamics under a tradeoff between survival and male display. These simulations indeed generate inversion-associated haplotypes with opposing sex-specific fitness effects. Antagonism strengthens with time, and can ultimately yield karyotypes at surprisingly predictable frequencies, with striking genotype frequency differences between sexes and between developmental stages. To test whether this model may contribute to well-studied yet enigmatic inversion polymorphisms in Drosophila melanogaster, we track inversion frequencies in laboratory crosses to test whether they influence male reproductive success or survival. We find that two of the four tested inversions show significant evidence for the tradeoff examined, with In(3 R)K favoring survival and In(3 L)Ok favoring male reproduction. In line with the apparent sex-specific fitness effects implied for both of those inversions, In(3 L)Ok was also found to be less costly to the viability and/or longevity of males than females, whereas In(3 R)K was more beneficial to female survival. Based on this work, we expect that balancing selection on antagonistically pleiotropic traits may provide a significant and underappreciated contribution to the maintenance of natural inversion polymorphism. |
| format | Article |
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| institution | OA Journals |
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| language | English |
| publishDate | 2025-04-01 |
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| spelling | doaj-art-a3b79eb90e3e42d9af091ef9a4e3748e2025-08-20T02:12:53ZengeLife Sciences Publications LtdeLife2050-084X2025-04-011210.7554/eLife.93338The potential of inversions to accumulate balanced sexual antagonism is supported by simulations and Drosophila experimentsChristopher S McAllester0https://orcid.org/0000-0002-4546-1009John E Pool1https://orcid.org/0000-0003-2968-9545Laboratory of Genetics, University of Wisconsin, Madison, United StatesLaboratory of Genetics, University of Wisconsin, Madison, United StatesChromosomal inversion polymorphisms can be common, but the causes of their persistence are often unclear. We propose a model for the maintenance of inversion polymorphism, which requires that some variants contribute antagonistically to two phenotypes, one of which has negative frequency-dependent fitness. These conditions yield a form of frequency-dependent disruptive selection, favoring two predominant haplotypes segregating alleles that favor opposing antagonistic phenotypes. An inversion associated with one haplotype can reduce the fitness load incurred by generating recombinant offspring, reinforcing its linkage to the haplotype and enabling both haplotypes to accumulate more antagonistic variants than expected otherwise. We develop and apply a forward simulator to examine these dynamics under a tradeoff between survival and male display. These simulations indeed generate inversion-associated haplotypes with opposing sex-specific fitness effects. Antagonism strengthens with time, and can ultimately yield karyotypes at surprisingly predictable frequencies, with striking genotype frequency differences between sexes and between developmental stages. To test whether this model may contribute to well-studied yet enigmatic inversion polymorphisms in Drosophila melanogaster, we track inversion frequencies in laboratory crosses to test whether they influence male reproductive success or survival. We find that two of the four tested inversions show significant evidence for the tradeoff examined, with In(3 R)K favoring survival and In(3 L)Ok favoring male reproduction. In line with the apparent sex-specific fitness effects implied for both of those inversions, In(3 L)Ok was also found to be less costly to the viability and/or longevity of males than females, whereas In(3 R)K was more beneficial to female survival. Based on this work, we expect that balancing selection on antagonistically pleiotropic traits may provide a significant and underappreciated contribution to the maintenance of natural inversion polymorphism.https://elifesciences.org/articles/93338pleiotropybalancing selectioninversionfrequency dependent selectionsexual antagonism |
| spellingShingle | Christopher S McAllester John E Pool The potential of inversions to accumulate balanced sexual antagonism is supported by simulations and Drosophila experiments eLife pleiotropy balancing selection inversion frequency dependent selection sexual antagonism |
| title | The potential of inversions to accumulate balanced sexual antagonism is supported by simulations and Drosophila experiments |
| title_full | The potential of inversions to accumulate balanced sexual antagonism is supported by simulations and Drosophila experiments |
| title_fullStr | The potential of inversions to accumulate balanced sexual antagonism is supported by simulations and Drosophila experiments |
| title_full_unstemmed | The potential of inversions to accumulate balanced sexual antagonism is supported by simulations and Drosophila experiments |
| title_short | The potential of inversions to accumulate balanced sexual antagonism is supported by simulations and Drosophila experiments |
| title_sort | potential of inversions to accumulate balanced sexual antagonism is supported by simulations and drosophila experiments |
| topic | pleiotropy balancing selection inversion frequency dependent selection sexual antagonism |
| url | https://elifesciences.org/articles/93338 |
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