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.
-
Whole genome resequencing of Capsella speciesEuropean Nucleotide Archive, PRJEB6689.
-
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.
Metrics
-
- 8,947
- views
-
- 798
- downloads
-
- 74
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Long-term balancing selection drives evolution of immunity genes in Capsella
eLife 8:e43606.
https://doi.org/10.7554/eLife.43606
Further reading
-
- Evolutionary Biology
Haldane’s rule occupies a special place in biology as one of the few ‘rules’ of speciation, with empirical support from hundreds of species. And yet, its classic purview is restricted taxonomically to the subset of organisms with heteromorphic sex chromosomes. I propose explicit acknowledgement of generalized hypotheses about Haldane’s rule that frame sex bias in hybrid dysfunction broadly and irrespective of the sexual system. The consensus view of classic Haldane’s rule holds that sex-biased hybrid dysfunction across taxa is a composite phenomenon that requires explanations from multiple causes. Testing of the multiple alternative hypotheses for Haldane’s rule is, in many cases, applicable to taxa with homomorphic sex chromosomes, environmental sex determination, haplodiploidy, and hermaphroditism. Integration of a variety of biological phenomena about hybrids across diverse sexual systems, beyond classic Haldane’s rule, will help to derive a more general understanding of the contributing forces and mechanisms that lead to predictable sex biases in evolutionary divergence and speciation.
-
- Evolutionary Biology
Living organisms control the formation of mineral skeletons and other structures through biomineralization. Major phylogenetic groups usually consistently follow a single biomineralization pathway. Foraminifera, which are very efficient marine calcifiers, making a substantial contribution to global carbonate production and global carbon sequestration, are regarded as an exception. This phylum has been commonly thought to follow two contrasting models of either in situ ‘mineralization of extracellular matrix’ attributed to hyaline rotaliid shells, or ‘mineralization within intracellular vesicles’ attributed to porcelaneous miliolid shells. Our previous results on rotaliids along with those on miliolids in this paper question such a wide divergence of biomineralization pathways within the same phylum of Foraminifera. We have found under a high-resolution scanning electron microscopy (SEM) that precipitation of high-Mg calcitic mesocrystals in porcelaneous shells takes place in situ and form a dense, chaotic meshwork of needle-like crystallites. We have not observed calcified needles that already precipitated in the transported vesicles, what challenges the previous model of miliolid mineralization. Hence, Foraminifera probably utilize less divergent calcification pathways, following the recently discovered biomineralization principles. Mesocrystalline chamber walls in both models are therefore most likely created by intravesicular accumulation of pre-formed liquid amorphous mineral phase deposited and crystallized within the extracellular organic matrix enclosed in a biologically controlled privileged space by active pseudopodial structures. Both calcification pathways evolved independently in the Paleozoic and are well conserved in two clades that represent different chamber formation modes.
