What have we figured out about social amoebas?

  • All three sexes (mating types) of Dictyostelium discoideum occur across eastern North America in roughly equal proportions. They are also all the same size, something called isogamy, meaning there is no sperm egg divergence, and also no cost of sex (Douglas et al. 2016).
  • Farmer clones of Dictyostelium discoideum that carry the bacterium Burkholderia make fewer sentinel cells, the cells that mop up toxins, bacteria and other harmful substances (functioning as a liver, kidney, and innate immune system) in the slug stage. Surprisingly, the farmers were no more vulnerable to toxins even without as many sentinel cells, so it appears the Burkholderia bacteria themselves help the amoebae in this way (Brock et al. 2016).
  • A review of kin discrimination in Dictyostelium shows that there is good evidence for kin recognition, but that it is not used for complete sorting. It may change actions in the social stage in other ways than sorting (Strassmann 2016).
  • Even tiny differences in spatial structure of a few centimeters can keep amoebae of different clones from finding each other and grouping together when starving (smith et al. 2016).
  • We collected Dictyostelium discoideum clones from nature and found that some carried Burkholderia and some did not. We then cured those carrying and infected those not carrying and found that some traits are co-evolved by Dictyostelium, and others are conferred by the bacteria. Short migration distance of the slugs, and carrying bacteria are conferred by the bacteria. Resistance to the harmful effects of bacteria and prudent harvesting are intrinsic to the amoebae (Brock et al. 2015).
  • Migration of the slug can impact social interactions in D. discoideum. We found that facultative cheating is reduced after migration, where it is defined as greater contribution to spore relative to stalk than found for that clone when clonal. Migration also reduced stalk height and chimeras migrated less far than pure clones. (Jack et al. 2015.
  • Burkholderia bacteria in two different Dictyostelium specific clades actually cause Dictyostelium to be able to carry bacteria. The Burkholderia themselves are generally not good food for Dicty, but facilitate the carriage of food bacteria in ways that the food bacteria alone cannot do. So the farming symbiosis we have discovered is initially caused by the bacteria. Subsequent co-evolution allows Dictyostelium clones that were collected with Burkholderia to avoid its negative consequences (DiSalvo et al. 2015).
  • We sequenced 20 clones of Dictyostelium discoideum and then compared genes identified as being involved in social cheating (getting more cells into spore than stalk) to other genes. We discovered that the social genes had higher levels of polymorphism in ways consistent with stalemate frequency dependent selection (Ostrowski et al. 2015).
  • We used Jennie Kuzdzal-Fick’s evolved populations at low relatedness to ask whether populations with obligate cheaters (cannot make stalk at all on their own) also evolved non-cheaters with defenses against cheaters. The answer was yes. Clones that evolved with cheaters were better able to defend against them than could naive clones (Levin et al. 2015).
  • We challenged 20 wild clones of D. discoideum with 32 clones of Escherichia coli and 1 clone of Klebsiella pneumoniae in a pairwise design to see if D. discoideum was harmed by the pathogenic E. coli clones, and whether this differed according to farmer status of the D. discoideum clones. We found that some of the E. coli clones were toxic to all D. discoideum, regardless of farmer status, though which ones could not be predicted from previous pathogenicity results. But this toxicity was reduced if the plate medium was more dilute, so bacteria could not reach high levels. The toxicity could also be overcome if we started with a lot of D. discoideum cells. This is called an Allee effect, that individuals to better in dense populations (DiSalvo et al. 2014).
  • We wondered whether the defensive Burkholderia carried by farmer clones of D. discoideum are protective against predation by nematodes and found that they were not, though this might not be true for all nematodes since there was a lot of variation between the two genera we tried – Caenorhabditis and Oscheius (Adu-Oppong et al. 2014).
  • The stalk of D. discoideum fruiting bodies is supposed to be to increase spore transport by animals (since spores are sticky, they would not be wind-transported). We tested this in the lab with Drosophila flies as movement agents and found they carried more spores of D. discoideum from atop stalks than when the stalks were knocked down (smith et al. 2014).
  • We found what might be the longest number of amino acid repeats in a gene ever. It is in D. discoideum and involves 306 tandem serine repeats in a functional gene (Tian et al. 2013).
  • In a mutation accumulation experiment, a clone is put through a single cell bottleneck for many generations. This reduces the effects of natural selection and lets new mutations prevail. It is an important kind of experiment for determining what traits are being maintained by natural selection, though this sort of experiment can only be done on organisms with short generation times amenable to laboratory culture. We found that most mutations had negative effects on fitness, as predicted, but some were beneficial.  Competitive ability in the social stage was under weak directional selection, indicating that wild clones are sometimes in competition with others. We found very low mutation rates also (Hall et al. 2013).
  • We were interested in two clones of the bacterium Pseudomonas fluorescens carried by D. discoideum. We knew they were two clones because they had different morphologies on a Petri plate. Also, one served as food for D. discoideum while the other did not. In collaboration with Pierre Stallforth from the Clardy lab, we discovered that the key difference between the two clones of P. fluorescens was that the edible one had a mutation in a major pathway that controlled many secretions (GacA). With that mutation it became edible and phylogeny analysis indicated that it was likely to have evolved from the other one, probably in the D. discoideum environment. Pierre also figured out that the difference between the two had to do with specific small molecules, with the inedible one making toxic chromene and pryrrolnitrate, and the edible one made siderophores, compounds that help bacteria get iron. The compounde of the inedible one helped its hosts grow while hurting non-hosts, thereby playing into the social amoeba conflict story. We wanted to put “guns and butter” in the title, but PNAS would not let us  (Stallforth et al. 2013).
  • It is a good idea to share methods for experiments in more detail than are usually found in papers. We did this with two of our main techniques, collecting clones from the wild, and competing different clones together in ways we hope are useful to other scientists (Buttery et al. 2013, Douglas et al. 2013).
  • We were puzzled by the Burkholderia bacteria carried by D. discoideum farmers that could not support growth. We wondered what was the advantage to the amoebae and wondered if it could be in competition with other clones. We tested this by adding supernatant from the bacteria and also by mixing amoeba clones with and without the bacteria and found that the bacteria and their supernatants functioned as weapons against the nonfarmers, causing them to win in competition to be spore not stalk (Brock et al. 2013).
  • One of the interesting questions you can ask is when during development genes are expressed. von Baer’s law expects the earliest genes to be the most conserved. Other studies suggest an hourglass pattern. We found the strongest conservation and weakest evolvability late in development, which supports the idea that there are spatial constraints in evolution of a body and that the lack of modularity in Dictyostelium gives rise to this pattern (Tian et al. 2013).
  • We identified a specific gene of unknown function we call chtB in D. discoideum which when knocked out causes excess representation in spore not stalk. There were no obvious fitness costs (Santorelli et al. 2013).
  • We sequenced three lines of a mutation accumulation experiment to get at the mutation rate of D. discoideum and found it to be exceptionally low, nuclear 2.9 x 10^-11 with a mitochondrial mutation rate of .76 x 10^-09. this is the lowest reported thus far for any eukaryote (Saxer et al. 2012).
  • D. discoideum has a lot of triplet repeats which can result in amino acid repeats. In this species they do so, mostly polyglutamine repeats, which are the same ones that cause neurological disorders like Huntington’s disease in humans. We found coding repeat loci to be about as variable as non-coding, indicating a lack of extra function (Scala et al. 2012).
  • Sometimes adaptive goals are achieved in organisms through more than one way. In the social amoeba Dictyostelium discoideum fruiting bodies are largely but not entirely uniclonal. We found that actual kin recognition accounts for a minor part of that fact, and co-occurrence or the lack of it is more important (Gilbert et al. 2012).
  • The structure of the environment is important in selecting for the attributes of organisms. In social amoebae, we found that stalked migrators like D. giganteum, or D. purpureum pay the cost of continuously generating stalks made up of dead cells, but this allows them to be able to cross small gaps in the soil, something D. discoideum cannot do, though it can profit from the stalks of other species and cross gaps (Gilbert et al. 2012).
  • We found that when a mixture of two clones grow out from one location, drift along the growing front accentuates differences among the clones, allowing one to displace the other, a neglected form of social competition (Buttery et al. 2012).
  • Altruism in a single Dictyostelium discoideum clone can be lost in 30 experimental evolution rounds at very low relatedness, but is not easily lost with even occasional single-cell bottlenecks (Kuzdzal-Fick et al. 2011).
  • Slug movement across a plate has different costs and benefits if there is a dead stalk during movement (Jack et al. 2011).
  • There are likely to be cryptic species basal to D. discoideum in the neotropics (Douglas et al. 2011).
  • Dictyostelium is an excellent model system for social evolution (review) (Strassmann et al. 2011).
  • Weaker cells are more likely to become stalk (Castillo et al. 2011).
  • The newly sequenced genome of D. purpureum indicates that social genes evolve rapidly (Sucgang et al. 2011).
  • Some clones of D. discoideum and other species have a symbiotic relationship with bacteria – farming – in which they carry bacteria though the spore stage and seed them out after dispersal (Brock et al. 2011).
  • D. discoideum has sexual recombination regularly, as indicated by recombination rates (Flowers et al. 2010).
  • The first cells to starve that call in the other cells become spore, not stalk, consistent with an advantage of being the first to turn on genes for competition  (Kuzdzal Fick et al. 2010).
  • Resistance against cheaters can be easily evolved, and these resistors are not themselves cheaters on wild-type (Khare et al. 2010)
  • We found a huge field in Texas containing a single, abundant clone of D. discoideum  (Gilbert et al. 2009).
  • Different clones can recognize each other and segregate during development; this is mediated by lagC and LagB (trgC and tgrB) genes, which are highly variable (Benabentos et al. 2009; Ostrowski et al. 2009; Mehdiabadi et al. 2006, 2009).
  • Sometimes two species form fruiting bodies together, but the fruiting bodies are not intermediate morphologically (Jack et al. 2008).
  • There are over a hundred knockouts that cause their bearers to cheat against intact clones suggesting that there are many factors contributing to sociality (Santorelli, et al. 2008).
  • A mutation accumulation experiment demonstrated that microsatellite mutation rates are extremely low in D. discoideum (McConnell et al. 2007).
  • Wild fruiting bodies have very high relatedness, sufficient to suppress costly cheaters (Gilbert et al. 2007).
  • As D. discoideum slugs move, they drop off cells capable of exploiting newly-found food sources (Kuzdzal-Fick et al. 2007).
  • Chimeras have a cost; they move less far than clones on agar and soil (Foster et al. 2002; Castillo et al. 2005).
  • An apparent cheater knock-out lost late in the social stage, because of pleiotropic effects, indicating that pleiotropy is a powerful stabilizer of cooperation (Foster et al. 2004).
  • Wild co-occurring clones form a linear dominance hierarchy in which the loser produces the fewest spores, and the most dead stalk cells (Fortunato et al. 2003a, 2003b).
  • We found a greenbeard gene that recognizes and favors others with the same gene (Queller et al. 2003).
  • Multiple clones join into the same fruiting body in social amoebae, where one clone contributes more than its fair share to spores (Strassmann et al. 2000).

More detail on some topics:

  • Multicellularity and social cheating in Dictyostelium discoideum: Social amoebae have a solitary stage in which they eat bacteria and divide by binary fission. They also have a multicellular stage that begins with aggregation, so genetically different clones can come together and compete to become spore and avoid being stalk. Different clones do co-aggregate and contribute differently to spore vs. stalk, establishing this as a good system to study social evolution (Strassmann et al. 2000).
  • Single-gene greenbeard effects in the social amoeba Dictyostelium discoideum: A greenbeard gene is one that combines a trait, its recognition, and an altruistic act all in one. It is something that W. D. Hamilton predicted, R. Dawkins named, and many thought impossible, because of the effects of such a gene on the rest of the genome. We identified a cell adhesion gene that functions as a greenbeard, and demonstrated its pleiotropic effects on the multicellular organism differed according to substrate.
  • Phylogeny of Dictyostelium: There are few morphological characters to sort social amoebae into species. It is very important for studies of social interactions to know if individuals are of the same or different species. Since we can freeze spores of Dictyostelium, and do experiments repeatedly on the same clones, it is worth the effort to put individual clones in a phylogeny. We have found that many clones of D. discoideum fall into one clade. We have also found that there are likely to be several cryptic species closely related to D. discoideum in the neotropics.
  • Agriculture in Dictyostelium We have discovered that several species of Dictyostelium have clones that carry bacteria through the social stage, then disperse them when the Dictyostelium  encounter conditions favorable for proliferation. There are multiple species of bacteria carried. Some are used for food, but some are not. Farmers are prudent in the sense that they enter the social stage before they have eaten all the bacteria. Much of our future research will follow this exciting development.
  • Organismality We have defined an organism in a new and conceptually cohesive way as having high cooperation and low conflict among its parts. This definition puts animals that develop through a single cell bottleneck as organisms, but also claims that some symbioses and other collaborations formerly not understood as organisms in fact are.
  • Cheating The multicellular stage of Dictyostelium begins with aggregation, setting the stage for one clone to force the other into becoming the dead stalk. We have defined three kinds of cheating, examined their frequency, and shown that under experimental evolution with very low relatedness, altruism can be lost.