Biologists ID molecular block for social ’cheaters’

Social cooperation is one of the most difficult adaptations for evolutionary biologists to explain because competition for resources inside the collective should lead to evolved traits that allow individuals to “cheat” the collective, win more resources and reproduce faster than their more cooperative neighbors — thus undermining the social collective. In new research, evolutionary biologists and geneticists at Rice University and Baylor College of Medicine have isolated a genetic mechanism that counters competitive pressures and stabilizes cooperation. Their research appears in the Oct. 7 issue of the journal Nature.


Using the latest tools of molecular genetics, the researchers found that the phenomenon known as pleiotropy — which occurs when a gene affects more than one inherited trait — plays a crucial role in preventing “cheaters” from exploiting their neighbors within slime mold colonies that are formed by the social amoeba Dictyostelium discoideum. “What we’ve found is a molecular block to cheating and the genetic mechanism it relies on– tying cooperative genes tightly with the essential function of reproduction,” said paper co-author Joan Strassmann, professor of ecology and evolutionary biology at Rice. “Such a mechanism makes the loss of social genes costly to cheaters, and we believe this pleiotropic mechanism may be indicative of a general mechanism that’s employed in many species to stabilize cooperation.”

The Rice-Baylor experiments draw upon one of the most extraordinary examples of social cooperation among microorganisms: when slime mold amoebae run out of the bacteria they eat, they group, then form a fruiting body in which about one-fifth of the single-celled individuals within the colony sacrifice themselves to form the stalk that holds up the spores. Before forming a stalk, the colony goes through a stage where it forms a slug-like structure. During this stage, cells produce a signaling molecule called DIF-1 that causes some members of the colony to differentiate themselves from the rest of the group and enter a prestalk stage of development. Using biotechnology, the research team created a mutant strain of Dictyostelium without the gene dimA, which codes for a key protein that Dictyostelium cells use to recognize DIF-1. “We wanted to see if cells without dimA could cheat the system by ignoring DIF-1 and thereby increase their chances of becoming spore cells rather than stalk cells,” said paper co-author David Queller, professor of ecology and evolutionary biology at Rice. “We created colonies that contained roughly a 50-50 mix of our mutants and wild type strains of Dictyostelium, As expected, the dimA knockouts — the cheaters — were predisposed to move to the back of the slug, the position occupied by cells in the prespore stage of development.”

But despite this advantage during stalk development, the cheaters were far less likely than their native counterparts to make it into the actual spores atop the stalk, a finding that surprised the entire research team. The researchers conducted a series of tests to determine whether the dimA mutants had an unexpected competitive disadvantage that was skewing the results of the experiment. One of those tests involved looking for a marker gene expressed only in prestalk cells. Using this marker gene, they determined that many cells in the spores were wild type cells that were initially tagged to become stalk cells. These cells underwent a late-stage developmental about-face and supplanted dimA knockout cells that were initially targeted to become spores.

“This test confirmed that the dimA gene was essential not only for DIF-1 recognition but also for spore production,” said paper co-author Gad Shaulsky, associate professor of molecular and human genetics at Baylor College of Medicine. “We don’t know the precise biomolecular pathway for this second function, but we know that dimA codes for a transcription factor that binds with DNA in the nucleus to control gene expression. Because transcription factors often control more than one gene, we believe the absence of dimA may be interfering with an unknown recognition pathway that is essential for spore selection.”

The results are the first published by a unique Rice-Baylor collaborative that won $5 million from the National Science Foundation last year to apply the latest techniques of modern molecular genetics and large-scale genomics to the study of social evolution. The project was one of the first funded by the NSF’s new Frontiers in Integrated Biological Research program.

Other co-authors on the paper, “Pleiotropy as a mechanism to stabilize cooperation,” are Kevin Foster, a former Huxley Fellow in ecology and evolutionary biology at Rice who is now a Fellow at the Wissenschaftkolleg in Berlin, and Chris Thompson, a former post-doctoral researcher at Baylor College of Medicine who is now at The University of Manchester.

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