Should we hail the Red King? Evolutionary consequences of a mutualistic lifestyle in genomes of lichenized ascomycetes
Abstract The Red Queen dynamic is often brought into play for antagonistic relationships. However, the coevolutionary effects of mutualistic interactions, which predict slower evolution for interacting organisms (Red King), have been investigated to a lesser extent. Lichens are a stable, mutualistic...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Wiley
2022-01-01
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| Series: | Ecology and Evolution |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/ece3.8471 |
| _version_ | 1828032256784990208 |
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| author | Claudio G. Ametrano H. Thorsten Lumbsch Isabel Di Stefano Ek Sangvichien Lucia Muggia Felix Grewe |
| author_facet | Claudio G. Ametrano H. Thorsten Lumbsch Isabel Di Stefano Ek Sangvichien Lucia Muggia Felix Grewe |
| author_sort | Claudio G. Ametrano |
| collection | DOAJ |
| description | Abstract The Red Queen dynamic is often brought into play for antagonistic relationships. However, the coevolutionary effects of mutualistic interactions, which predict slower evolution for interacting organisms (Red King), have been investigated to a lesser extent. Lichens are a stable, mutualistic relationship of fungi and cyanobacteria and/or algae, which originated several times independently during the evolution of fungi. Therefore, they represent a suitable system to investigate the coevolutionary effect of mutualism on the fungal genome. We measured substitution rates and selective pressure of about 2000 protein‐coding genes (plus the rDNA region) in two different classes of Ascomycota, each consisting of closely related lineages of lichenized and non‐lichenized fungi. Our results show that independent lichenized clades are characterized by significantly slower rates for both synonymous and non‐synonymous substitutions. We hypothesize that this evolutionary pattern is connected to the lichen life cycle (longer generation time of lichenized fungi) rather than a result of different selection strengths, which is described as the main driver for the Red Kind dynamic. This first empirical evidence of slower evolution in lichens provides an important insight on how biotic cooperative interactions are able to shape the evolution of symbiotic organisms. |
| first_indexed | 2024-04-10T15:02:58Z |
| format | Article |
| id | doaj.art-4c45c1d436834a67a9f144e20b6351da |
| institution | Directory Open Access Journal |
| issn | 2045-7758 |
| language | English |
| last_indexed | 2024-04-10T15:02:58Z |
| publishDate | 2022-01-01 |
| publisher | Wiley |
| record_format | Article |
| series | Ecology and Evolution |
| spelling | doaj.art-4c45c1d436834a67a9f144e20b6351da2023-02-15T09:06:07ZengWileyEcology and Evolution2045-77582022-01-01121n/an/a10.1002/ece3.8471Should we hail the Red King? Evolutionary consequences of a mutualistic lifestyle in genomes of lichenized ascomycetesClaudio G. Ametrano0H. Thorsten Lumbsch1Isabel Di Stefano2Ek Sangvichien3Lucia Muggia4Felix Grewe5Grainger Bioinformatics Center and Negaunee Integrative Research Center, Science and Education Field Museum of Natural History Chicago Illinois USAGrainger Bioinformatics Center and Negaunee Integrative Research Center, Science and Education Field Museum of Natural History Chicago Illinois USAGrainger Bioinformatics Center and Negaunee Integrative Research Center, Science and Education Field Museum of Natural History Chicago Illinois USADepartment of Biology Faculty of Science Ramkhamhaeng University Bangkok ThailandUniversity of Trieste Trieste ItalyGrainger Bioinformatics Center and Negaunee Integrative Research Center, Science and Education Field Museum of Natural History Chicago Illinois USAAbstract The Red Queen dynamic is often brought into play for antagonistic relationships. However, the coevolutionary effects of mutualistic interactions, which predict slower evolution for interacting organisms (Red King), have been investigated to a lesser extent. Lichens are a stable, mutualistic relationship of fungi and cyanobacteria and/or algae, which originated several times independently during the evolution of fungi. Therefore, they represent a suitable system to investigate the coevolutionary effect of mutualism on the fungal genome. We measured substitution rates and selective pressure of about 2000 protein‐coding genes (plus the rDNA region) in two different classes of Ascomycota, each consisting of closely related lineages of lichenized and non‐lichenized fungi. Our results show that independent lichenized clades are characterized by significantly slower rates for both synonymous and non‐synonymous substitutions. We hypothesize that this evolutionary pattern is connected to the lichen life cycle (longer generation time of lichenized fungi) rather than a result of different selection strengths, which is described as the main driver for the Red Kind dynamic. This first empirical evidence of slower evolution in lichens provides an important insight on how biotic cooperative interactions are able to shape the evolution of symbiotic organisms.https://doi.org/10.1002/ece3.8471coevolutioncomparative genomicsevolutionary ratelichenized fungiPyrenulalesTrypetheliales |
| spellingShingle | Claudio G. Ametrano H. Thorsten Lumbsch Isabel Di Stefano Ek Sangvichien Lucia Muggia Felix Grewe Should we hail the Red King? Evolutionary consequences of a mutualistic lifestyle in genomes of lichenized ascomycetes Ecology and Evolution coevolution comparative genomics evolutionary rate lichenized fungi Pyrenulales Trypetheliales |
| title | Should we hail the Red King? Evolutionary consequences of a mutualistic lifestyle in genomes of lichenized ascomycetes |
| title_full | Should we hail the Red King? Evolutionary consequences of a mutualistic lifestyle in genomes of lichenized ascomycetes |
| title_fullStr | Should we hail the Red King? Evolutionary consequences of a mutualistic lifestyle in genomes of lichenized ascomycetes |
| title_full_unstemmed | Should we hail the Red King? Evolutionary consequences of a mutualistic lifestyle in genomes of lichenized ascomycetes |
| title_short | Should we hail the Red King? Evolutionary consequences of a mutualistic lifestyle in genomes of lichenized ascomycetes |
| title_sort | should we hail the red king evolutionary consequences of a mutualistic lifestyle in genomes of lichenized ascomycetes |
| topic | coevolution comparative genomics evolutionary rate lichenized fungi Pyrenulales Trypetheliales |
| url | https://doi.org/10.1002/ece3.8471 |
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