Friday, December 2, 2011

Amoebal behavior by Maria Rebolleda-Gomez

It is common to see documentaries on television about animal behavior. We have all seen lions trying to catch zebras in African savannas, learned about the social structure of ant communities and the reproductive behavior of the birds of paradise. However (in general) we know almost nothing about the behavior of amoebas. In the past few years, nonetheless, some attention has been given to the complex behavior of the social amoeba: Dictyostelium discoideum. This amoeba is not only worthy of an exciting documentary about wildlife, but is a great model to understand social interactions such as cooperation.

Figure 1. Life cycle of D. discoideum 
(reproduced from Strssmann and Queller, 2011).
D. discoideum belongs to the slime molds or social amoebas group. There are over 100 species of Dictyostelium, however the best-studied one is D. discoideum. This amoeba has a complicated life cycle with both unicellular and multicellular life stages (Figure 1). During the unicellular stage of their life cycle, individual amoebas live in the soil where they feed on bacteria. The scenario here is not the African Savanna, the predator is D. discoideum and there are bacteria instead of zebras. However, not even during this stage are these amoebas completely alone. These small predators are always capable of sensing the density of nearby amoeba and respond accordingly (Strassmann and Queller, 2011). When feeding in the soil D. discoideum cells secrete a molecule called the “prestarvation factor”. This is an autocrine factor that accumulates as a function of cell density and triggers the expression of genes whose products have an important role in the transition to a multicellular stage. However, the onset of this response is inhibited in a density dependent manner by the presence of the bacteria Klebisiella aerogenes. As a result, the transition to the multicellular stage requires a low availability of food (bacterial density) and a high cellular density of D. discoideum (Burdine and Clarke, 1995).

In response to these signals, when bacteria are scarce and amoeba density has reached a certain threshold, D. discoideum enter one of two stages: the sexual or social stage. During the social stage amoebas aggregate following a cAMP gradient produced by the cells themselves. A multicellular slug forms and cells differentiate in such way that the tip becomes the anterior extreme and organizes the movement towards light and away from ammonia. During movement some posterior cells detach from the slug allowing exploitation of bacterial rich patches (Kuzdzal-Fick et al., 2007; Strassmann and Queller, 2011).

Eventually, the anterior cells migrate down towards the center of the aggregate to initiate fruiting body formation. The aggregate differentiates in a stalk (20% of the cells) and a spore ball at the tip (80% of the cells). In this division, stalk cells die forming a cellulose wall that confers the strength for holding the spores, allowing for spore dispersion. This division then involves the sacrifice of the stalk cells for the spore cells survival, and is, therefore, of behavioral interest (Strassmann and Queller, 2011). The social stage is also of behavioral interest but is a topic for another blog entry.

The reason why altruism is such an interesting phenomenon is because it defies evolutionary understanding. The problem with altruism is to understand how can it be stably maintained in the face of cheaters (individuals that obtain the benefits without paying the cost). If a cheater appears in the population (by mutation, migration or any other means) it will have more descendants that would probably be cheaters as well. The population will collapse and altruism will not be maintained. Evolutionary biologists have been aware of this problem for a long time, and different factors have been proposed as promoters of altruism evolution (or at least helping to prevent cheating).

Kin Selection
Imagine however that cooperators only cooperate with their close relatives, enhancing the survival of other individuals with a high probability of being cooperators as well. Cheaters will not spread in the population because cooperative behavior between cooperators will enhance their fitness. If a cheater mutant arises in one of such groups, it will not be able to spread because its close relatives will also have a high probability of being cheaters. In order to be successful, cheaters need cooperators to cheat; it is not possible to copy in an exam if everybody is also copying (Actually, the success of the cheaters directly depends on how many people really studied for that test). William D. Hamilton (1964) formalized this model of kin selection as an explanation for cooperative traits. He proposed that cooperative traits could spread in the population if:


where r is the degree of relatedness of cooperator entities (the actor and the recipient), B is the benefit for the cooperator and C the cost of the interaction. In short, direct and indirect benefits (benefits for my kin) need to exceed the costs. Nevertheless, some hypotheses and details about this theory (in particular those concerning the evolutionary outcomes) have been difficult to test due to long generation times of species, as well as the difficulty to control different variables.

D. discoideum as a model organism for the evolution of cooperation
In this sense, D. discoideum is ideal to study evolution of cooperative traits. It has a cooperative life cycle, is small and easy to manipulate in lab conditions, and has a short generation time. In addition, there are many genetic tools developed for this organism including a fully sequenced genome! As far as testing cooperation, one of the first questions to ask is, can D. discoideum recognize its kin? One could expect some sort of recognition because different strains might coexist in the soil and the cost of cooperation is huge (you either die or reproduce). In other words it would not be evolutionary convenient to associate with unrelated strains during the social stage.

Figure 2. Proportion of fluorescent
spores relative to a mean value.
Ostrowski and collaborators addressed this question in 2008. In this study a reference fluorescence strain was mixed with either closely or distant related strains in a one to one proportion. These mixed cultures were grown on conditions promoting the development of the fruiting body (see life cycle). After the formation of this structure, the proportion of fluorescent (reference strain) and non-fluorescent strains was determined for each fruiting body and then compared across treatments. As the genetic distance between isolates is increased (from genetically identical, to slightly distant, to distantly related) the proportion of fluorescent/non-fluorescent spores diverges from a mean value. In other words, there are less mixed fruiting bodies as the genetic distance between the isolates increases (Figure 2).

D. discoideum is definitively an organism worth of a nature documentary, but further more is a valuable organism to our understanding of cooperation and its evolution. This essay is not intended to be an extensive review, but in terms of cooperation there is still much to say about this amoeba.

Burdine, V. and M. Clarke. 1995. Genetic and physiologic modulation of the prestarvation response in Dyctiostellium discoideum. Mol Biol Cell. 6(3):311-325
Hamilton, W. D.1964. The genetical evolution of social behaviour. I. J Theor Biol 7:1–16.
Kuzdzal-Fick, J.J., K. R. Foster, D. C. Queller and J. E. Strassmann. 2007. Exploiting new terrain: an advantage to sociality in the slime mold Dictyostelium discoideum. Behavioral Ecology: 433-437
Ostrowski E.A., M. Katoh, G. Shaulsky, D. C. Queller and J. E. Strassmann .2008. Kin discrimination increases with genetic distance in a social amoeba. PLoS Biol 6:e287.
Strassmann, J. E. and D. C. Queller. 2011. Evolution of cooperation and control of cheating in a social microbe. PNAS 108(2): 1085510862

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