MyxoEE-2

Cheating Limits

Conducted 2001-2002

Background

Individuals often differ greatly in how much energy they spend on behavior that benefits others. Such variation raises questions about how genetic differences between individuals that cause large differences in cooperation-investment can coexist for long periods, and how and why their frequencies fluctuate.

MyxoEE-2 was designed to i) test whether M. xanthus “cooperators” and “cheaters” would co-exist over several cycles of growth and development in well-mixed populations due to frequency-dependence of their fitness ranks, and ii) examine whether distinct cheaters co-cultured with the same cooperator after starting at the same frequency might diverge in their population dynamics and in their effects on cooperator and total-population dynamics.

MyxoEE-2 was not originally designed to study evolution caused by new mutations arising during the experiment. But a fascinating mutation-driven phenotypic transition emerged - a cheater mutated into a new cooperation-proficient genotype named Phoenix. Intriguingly, Phoenix’s parent genotype - which cheats on the cooperator used to initiate MyxoEE-2 - is unable to cheat on Phoenix. Pursuit of Phoenix’s molecular origin motivated the first use of next-generation sequencing in evolutionary biology.

Design summary - Three gentically distinct cheaters were used. Cheaters are defective at making social signal molecules necessary for development and thus make no or few spores when starving in monoculture. But in co-culture with developmentally proficient strains (cooperators), cheaters exploit signal molecules produced by the cooperators to make proportionally more spores than the cooperators. The population dynamics of cocultured cheaters and cooperators - which began as 1% and 99% of the starting populations, respectively - were characterized over five successive cycles of population growth in nutrient-rich broth followed by five days of starvation on buffered agar plates, conditions that induce fruiting-body development and sporulation for strains proficient at those traits.

Highlights

Frequency-dependent selection co-maintains cooperation and cheating - Frequency dependence of social-fitness ranks allows some cooperators and cheaters to coexist for extended periods.

Cheating can cause its own extinction due to cheating load - Population crashes caused by cheating can lead to cheater extinction while cooperators persist.

Cheating facilitates an evolutionary transition from cheaters to cheating-resistant cooperators - Cooperation by a developmentally-proficient cooperator strain toward an obligately defective cheater allows an evolutionary transformation of the cheater into a new type of cooperator to occur. The new cooperator displaces the original cooperator and is resistant to cheating.

Evolutionary biology meets next-generation sequencing - Next-generation sequencing is used to investigate evolutionary questions for the first time. Mutations potentially responsible for the evolutionary degradation and subsequent re-evolution of cooperation in a bacterial lineage are identified.

A small RNA and its regulatory pathway control myxobacterial development - Analysis of a mutation unique to a re-evolved cooperator — Phoenix — reveals a small RNA named Pxr and an associated regulatory pathway that together regulate initiation of M. xanthus development as a function of nutrient level. 2010, 2014, 2016, 2017a, 2017b, 2019, 2023.

Publications

Fiegna, F. and G. J. Velicer. 2003. Competitive fates of bacterial social parasites: persistence and self-induced extinction of Myxococcus cheaters. Proceedings of the Royal Society B. READ IT HERE

Fiegna, F., Y.-T. N. Yu, S. V. Kadam and G. J. Velicer. 2006. Evolution of an obligate social cheater to a superior cooperator. Nature. READ IT HERE

Velicer, G. J., G. Raddatz, H. Keller, S. Deiss, C. Lanz, I. Dinkelacker and S. C. Schuster. 2006. Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proceedings of the National Academy of Sciences USA. READ IT HERE

Kadam, S. V., S. Wegener-Feldbrügge, L. Søgaard-Andersen and G. J. Velicer. 2008.  Novel transcriptome patterns accompany evolutionary reversion of defective social development in the bacterium Myxococcus xanthus. Molecular Biology and Evolution. READ IT HERE

Yu, Y.-T. Y., X. Yuan and G. J. Velicer. 2010. Adaptive evolution of an sRNA that controls Myxococcus development. Science. READ IT HERE

Chen, I.-.C. K., B. Griesenauer, Y.-T. N. Yu and G. J. Velicer. 2014. A recent evolutionary origin of a bacterial small RNA that controls multicellular fruiting body development. Molecular Phylogenetics and Evolution. READ IT HERE

Yu, Y.-T.N., M. Kleiner and G. J. Velicer. 2016. Spontaneous reversions of an evolutionary trait loss reveal regulators of an sRNA that controls multicellular development in the myxobacteria. Journal of Bacteriology. READ IT HERE

Yu, T.-T.N., E. Cooper and G. J. Velicer. 2017. A conserved stem of the Myxococcus xanthus sRNA Pxr controls sRNA accumulation and multicellular development. Scientific Reports. READ IT HERE

Chen, I.-.C. K., G. J. Velicer and Y.-T.N. Yu. 2017. Divergence of functional effects among bacterial sRNA paralogs. BMC Evolutionary Biology. READ IT HERE

Chen, I.-C. K., B. M. Satinsky, G. J. Velicer and Y.-T.N. Yu. 2019. sRNA‐pathway genes regulating myxobacterial development exhibit clade‐specific evolution. Evolution & Development. READ IT HERE

Cossey, S. M.,  G. J. Velicer and Y.-T. N Yu. 2023. Ribonuclease D processes a small RNA regulator of multicellular development in myxobacteria. Genes. READ IT HERE