We are interested in multicellularity and social evolution, in genes that promote cooperation, in how conflict is controlled, and in the kinds of environmental structures that favor cooperation and multicellularity. We view organisms as entities where actual cooperation is paramount and conflict is controlled. Our research centers on social amoebae, particularly Dictyostelium discoideum, though we have a great deal of experience with social wasps and stingless bees. We use techniques from cell biology, genomics, population genetics, phyogenetics, and experimental evolution, and we collaborate freely.
Multicellularity, cooperation, and conflict in Dictyostelium
- How does chimerism limit multicellularity?
- What kinds of cheating occur in multicellular organisms formed by aggregation?
- How is cheating controlled?
- How do genes involved in the social stage evolve?
- What kinds of population structures prevent cheating?
- Can we grow Dictyostelium under different artificial life cycles to ask when cheating is a problem even for clonal organisms?
Sexual reproduction in Dictyostelium discoideum
- Are there more than four sexes in Dictyostelium discoideum?
- What are the frequencies of the sexes in interbreeding populations?
- Is there cheating in the sexual stage?
Dictyostelium discoideum systematics
- Are there closely related undescribed species in the neotropics?
Kin recognition in social amoebae
- Now we know genes involved in recognition, how do they function in nature?
- Are there passive forces like drift that result in lineage sorting?
- Is sorting the only form of recognition or can clones tell when they end up in chimeras, then expoit non-relatives?
- Can we test Crozier’s paradox that kin recognition removes the very genetic cues it requires?
- What bacteria are symbiotic with Dictyostelium; are some unculturable?
- What are the genetic differences between Dictyostelium farmers, and non-farmers?
- What are the genetic differences between symbiotic bacteria and independent bacteria?
- What small molecules are involved in the symbiosis?
- How do farmers benefit from carrying bacteria?
- Do farmers suffer costs from being tolerant of bacteria?
- How do bacteria benefit from the symbiosis?
- What keeps the symbiosis cooperative?
- Are bacteria protective against predators like nematodes?
Molecular evolution and genomics in Dictyostelium
- Do social genes evolve rapidly in conflict-drive arms races?
- Is there more balancing selection on social genes (e.g. stable ESS)?
- Is there a molecular signature of direct versus indirect kin selection?
- Can patterns of purifying selection on different classes of genes tell us what is important in Dictyostelium’s natural enviroment?
- Does Dictyostelium have an intermediate stage in development that is most conserved, as in animals?
- What will new genomes of four species and 20 resequenced genomes tell us?
- Why does Dictyostelium have so many short tandem repeats (microsatellites)?
- Can we detect recent selective sweeps, for example of cheating genes?
- What is the mutation rate, both at the DNA level and the phenotypic level?
- Is there micro- or macro-geographic population structure in D. disoideum?
- What are the patterns of linkage disequilibrium?
More detail on some of our projects:
NSF DEB0918931 Kin Recognition: Altruism and cooperation are fundamental to some of the major transitions in the history of life. Kin recognition is a vital part of cooperation and altruism; it ensures that altruistic benefits go to those who share the altruism allele, and it helps to limit cheaters, those who would gain the benefits of cooperation without paying the costs. Recently, it has been realized that altruism and cooperation occur in a number of microbial taxa. The experimental tractability of some of these taxa, in terms of both ease of lab culture and genetic manipulation, offer exciting opportunities to probe social evolution questions in new ways. We propose to study kin recognition in the social amoeba Dictyostelium discoideum, having recently discovered that, to varying degrees, distinct clones sort into separate cooperative fruiting bodies. The degree of sorting is correlated with genetic distance of the clones mixed. We will pursue this finding in four directions. First we will characterize recognition in a broader set of clones, and use those results to test costs and benefits of recognition. For example, we will test how well recognition protects against cheaters, using our unique collection of over 100 cheater knockout mutants. Second, we will determine if recognition is used to cheat when clones do mix. Again our collection of cheater mutants is valuable. Genes that cause cheating when knocked out (i.e. cooperation genes) are predicted be used to cheat in mixtures via downregulation. We will also test the converse prediction that genes upregulated in mixtures will be victims when knocked out (i.e. cheating genes). Third, we will search for genes involved in detecting kin using both a selection strategy and a population-genetic strategy. The latter involves finding genes that are highly polymorphic, and then conducting tests for molecular signatures of balancing selection. Finally, the candidate genes identified will be tested for whether they are actually associated with sorting. The many resources and tools available for D. discoideum make it likely that this work will make it the best understood kin recognition system in microbes, and the best characterized kin recognition system at the genetic level in any organism. This work will open up unique future opportunities. For example, one can construct clones that differ only in specified recognition alleles and conduct well-defined experiments to follow how kin recognition loci are selected in vivo.
NSF DEB1011513 Molecular evolution of social genes: The last few decades have seen revolutionary advances in the fields of molecular evolution and social evolution. The two have rarely been considered together, because the genes underlying social evolution are usually unknown. Yet social interactions may be an important driver of patterns of molecular variation. Social conflict may involve arms races that drive species differences and frequency-dependent selection that maintains variation within species. We will use the social amoeba Dictyostelium discoideum as a model system to test the hypothesis that conflicts in cooperative systems generate strong selection, and that this drives exceptional patterns of molecular variation, both within and between species. This species offers special advantages because of its prominent cooperative behavior and its rich genomic tools, including a sequenced genome and our development of a large and unique set of single-gene mutants that win in social conflict (“cheaters”). We will test our hypothesis test in two ways. Goal one is to define the fitness consequences of social variants in our pool of insertional mutant cheaters and in naturally varying clones. We will include tests of the factors thought to limit selection for cheaters, including frequency dependence, G x E interactions, relatedness, and pleiotropy. Goal two is to trace the consequences of social competition for molecular evolution, using wholegenome resequencing of multiple strains. We will test social genes (and control genes) for positive selection, guided by the hypothesis that social conflict drives arms races. We will also test for balancing selection, which is expected when the gains from cheating decline as cheater frequency increases. To confirm the role of social selection, we will test the social effects of key sequences, including inferred ancestral sequences, by inserting them into the lab strain Ax4. This work will test general principles of social evolution that are central to major evolutionary transitions like the evolution of cells, the evolution of eukaryotes, and the evolution of multicellularity.
Social amoebae – bacteria interactions. We have recently discovered that about a third of social amoeba clones carry bacteria through the social stage and then farm them out and consume them, as we would care for and then eat chickens or sheep. Other carried bacteria apparently function as weapons against other clones. This all-microbial symbiosis has great potential for understanding eukaryote interactions at the interface between benefit and pathogenesis. We are pursuing a variety of questions and approaches.
Genomics. We have recently sequenced four new genomes of Dictyostelids, and have also resequenced 20 D. discoideum genomes. We are now using these to test for adaptive evolution and arms races. We are also looking at patterns of purifying selection to ask about Dicty in its natural environment: what kinds of bacteria is it adapted to and how often does it go through the social and sexual cycles.
Experimental evolution. One of the advantages of a microbial system is that it is amenable to hypothesis testing using experimental evolution. Our most recent study along those lines demonstrated that altruism could be lost in as few as 30 rounds of fruiting body formation, if relatedness is sufficiently low. This provides strong support for the theory of kin selection. We are using this technique to look at a variety of other aspects of Dictyostelium behavior, and we are characterizing the newly-evolved selfish mutants.
Dictyostelium phylogenetics. Social interactions within species have different characteristics compared to interactions between species, so it is important to know if interacting pairs belong to the same species. We have published a phylogeny of Dictyostelium discoideum and closely related clones, and are working on close relatives to this species from the neotropics.
Dictyostelium sex. The sexual process involves meiosis, like any good eukaryote. It also involves cannibalism, a great deal of recombination, and at least four mating types. This is a rich area for exploring the interface between sociality, cheating, and sex.