Conditional expression explains molecular evolution of social genes in a microbe

Janaina Lima de Oliveira, Atahualpa Castillo Morales, Balint Stewart, Nicole Gruenheit, Jennifer Engelmoer, Suzanne Battom Brown, Reinaldo A. de Brito, Laurence D. Hurst, Araxi O. Urrutia, Christopher R.L. Thompson, Jason B. Wolf

Research output: Contribution to journalArticlepeer-review

18 Citations (SciVal)

Abstract

Conflict is thought to play a critical role in the evolution of social interactions by promoting diversity or driving accelerated evolution. However, despite our sophisticated understanding of how conflict shapes social traits, we have limited knowledge of how it impacts molecular evolution across the underlying social genes. Here we address this problem by analyzing the genome-wide impact of social interactions using genome sequences from 67 Dictyostelium discoideum strains. We find that social genes tend to exhibit enhanced polymorphism and accelerated evolution. However, these patterns are not consistent with conflict driven processes, but instead reflect relaxed purifying selection. This pattern is most likely explained by the conditional nature of social interactions, whereby selection on genes expressed only in social interactions is diluted by generations of inactivity. This dilution of selection by inactivity enhances the role of drift, leading to increased polymorphism and accelerated evolution, which we call the Red King process.

Original languageEnglish
Article number3284
Pages (from-to)1-12
Number of pages12
JournalNature Communications
Volume10
Issue number1
DOIs
Publication statusPublished - 23 Jul 2019

Funding

This work was funded by grants from the Biotechnology and Biological Sciences Research Council (BBSRC) (BB/M01035X/1; BB/M007146/1) to J.B.W., L.D.H., and C.R. L.T., the Natural Environment Research Council (NE/H020322/1) to J.B.W. and C.R.L. T., the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2014-50698-7) to R.A.B., a Wellcome Trust Investigator Award (WT095643AIA) to C.R.L.T, a BBSRC studentship to S.B., and a studentship from CNPq (234216/2014-0) to J.L.O. J.B.W. completed some of this work as a fellow at the Wissenschaftkolleg zu Berlin. We thank: Mike Wade for critical discussions that motivated this work, Joan Strassmann, Dave Queller and Michael Purugganan for discussions during the development of this work, Carlos Congrains for help with the implementation of the computational components.

ASJC Scopus subject areas

  • General Chemistry
  • General Biochemistry,Genetics and Molecular Biology
  • General Physics and Astronomy

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