Long-term balancing selection drives evolution of immunity genes in Capsella
- Max Planck Institute for Developmental Biology, Germany
- Stockholm University, Sweden
- University of Osnabrück, Germany
Abstract
Genetic drift is expected to remove polymorphism from populations over long periods of time, with the rate of polymorphism loss being accelerated when species experience strong reductions in population size. Adaptive forces that maintain genetic variation in populations, or balancing selection, might counteract this process. To understand the extent to which natural selection can drive the retention of genetic diversity, we document genomic variability after two parallel species-wide bottlenecks in the genus Capsella. We find that ancestral variation preferentially persists at immunity related loci, and that the same collection of alleles has been maintained in different lineages that have been separated for several million years. By reconstructing the evolution of the disease related locus MLO2b, we find that divergence between ancient haplotypes can be obscured by referenced based re-sequencing methods, and that trans-specific alleles can encode substantially diverged protein sequences. Our data point to long term balancing selection as an important factor shaping the genetics of immune systems in plants and as the predominant driver of genomic variability after a population bottleneck.
Data availability
All raw sequencing data are depsoited under the accession codes PRJEB6689.
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Whole genome resequencing of Capsella speciesEuropean Nucleotide Archive, PRJEB6689.
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Capsella grandiflora WGSEuropean Nucleotide Archive, PRJEB6689.
Article and author information
Author details
Funding
European Research Council (IMMUNEMESIS)
- Detlef Weigel
Human Frontier Science Program (LT000783/2010-L)
- Daniel Koenig
Deutsche Forschungsgemeinschaft (WE 2897/4-2)
- Detlef Weigel
Max-Planck-Gesellschaft (Open-access funding)
- Detlef Weigel
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2019, Koenig et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Long-term balancing selection drives evolution of immunity genes in Capsella
eLife 8:e43606.
https://doi.org/10.7554/eLife.43606
Further reading
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- Evolutionary Biology
A major question in animal evolution is how genotypic and phenotypic changes are related, and another is when and whether ancient gene order is conserved in living clades. Chitons, the molluscan class Polyplacophora, retain a body plan and general morphology apparently little changed since the Palaeozoic. We present a comparative analysis of five reference quality genomes, including four de novo assemblies, covering all major chiton clades, and an updated phylogeny for the phylum. We constructed 20 ancient molluscan linkage groups (MLGs) and show that these are relatively conserved in bivalve karyotypes, but in chitons they are subject to re-ordering, rearrangement, fusion, or partial duplication and vary even between congeneric species. The largest number of novel fusions is in the most plesiomorphic clade Lepidopleurida, and the chitonid Liolophura japonica has a partial genome duplication, extending the occurrence of large-scale gene duplication within Mollusca. The extreme and dynamic genome rearrangements in this class stands in contrast to most other animals, demonstrating that chitons have overcome evolutionary constraints acting on other animal groups. The apparently conservative phenome of chitons belies rapid and extensive changes in genome.
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- Evolutionary Biology
- Genetics and Genomics
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.
