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Parallel evolution of the G protein-coupled receptor GrlG and the loss of fruiting body formation in the social amoeba Dictyostelium discoideum evolved under low relatedness

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Walker, Laura M, Sherpa, Rintsen N, Ivaturi, Sindhuri, Brock, Debra A, Larsen, Tyler J, Walker, Jason R, Strassmann, Joan E, Queller, David C·2023·G3: Genes, Genomes, Genetics
DOI 10.1093/g3journal/jkad235PMC PMC10755179

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Abstract

Aggregative multicellularity relies on cooperation among formerly independent cells to form a multicellular body. Previous work with Dictyostelium discoideum showed that experimental evolution under low relatedness profoundly decreased cooperation, as indicated by the loss of fruiting body formation in many clones and an increase of cheaters that contribute proportionally more to spores than to the dead stalk. Using whole-genome sequencing and variant analysis of these lines, we identified 38 single nucleotide polymorphisms in 29 genes. Each gene had 1 variant except for grlG (encoding a G protein-coupled receptor), which had 10 unique SNPs and 5 structural variants. Variants in the 5′ half of grlG—the region encoding the signal peptide and the extracellular binding domain—were significantly associated with the loss of fruiting body formation; the association was not significant in the 3′ half of the gene. These results suggest that the loss of grlG was adaptive under low relatedness and that at least the 5′ half of the gene is important for cooperation and multicellular development. This is surprising given some previous evidence that grlG encodes a folate receptor involved in predation, which occurs only during the single-celled stage. However, non-fruiting mutants showed little increase in a parallel evolution experiment where the multicellular stage was prevented from happening. This shows that non-fruiting mutants are not generally selected by any predation advantage but rather by something—likely cheating—during the multicellular stage.

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Metadata

Authors
Walker, L. M., Sherpa, R. N., Ivaturi, S., Brock, D. A., Larsen, T. J., Walker, J. R., Strassmann, J. E., & Queller, D. C.
Affiliations
  • Washington University in St. Louis (US)
  • University of Michigan (US)
Corresponding author
Walker, Laura M
ORCID
Venue
G3: Genes, Genomes, Genetics
Publisher
Oxford University Press (OUP)
Published
2023-10-13
Volume
14
Issue
1
ISSN
2160-1836 (ISSN-L)
DOI
10.1093/g3journal/jkad235
PMC
PMC10755179
OpenAlex
W4387606776
Cited by
2
References
3
Citations by year
2025: 1 · 2023: 1
FWCI
0.33
Type
journal article
Language
en
Open access
Licence
Locations
  • G3 Genes Genomes Genetics (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Science Foundation (IOS 16-56756, DEB 17-53743, DEB 22-37266)
  • McDonnell Genome Institute
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Social Sciences › Sociology and Political Science › Evolutionary Game Theory and Cooperation
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Protist diversity and phylogeny
Keywords
Dictyostelium discoideum, G protein-coupled receptors, fruiting body formation, experimental evolution, multicellularity, cheating, cooperation, single nucleotide polymorphisms, structural variants, folate receptor, parallel evolution, multicellular development
MeSH terms
Amoeba, Dictyostelium, Biological Evolution, Reproduction

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