TLS on Social Amoebae

The perfection of slugs

by Laurence D. Hurst



The humble cellular slime mould can tell us why slugs move their tails to their heads – and how altruism pays Laurence D. Hurst 1 Comment
Recommend? (16) How evolution by natural selection could give rise to the specialist morphology of worker ants, when these leave no offspring, was a problem for Darwin. He might as well have been worried about his own body. Like sterile workers, each cell in the body specializes to do its own thing, be it brain, bone, kidney or colon. With one exception, the cells of your body are as genetically dead as a sterile worker. Just as the queen ant is the only female in the colony with a genetic future, so too it is uniquely sperm or eggs that contribute directly to the next generation. So how come we have sterile worker ants and sterile worker cells?

Part of the answer to both of these problems was provided by W. D. Hamilton’s theory of altruism mediated by kin selection. He argued that helping makes evolutionary sense if the beneficiary is a relative: their genetic future is, in part, your genetic future. Ant hills are one large family. The cells of your body are even more closely related: they are identical clones, all derived from the same fertilized egg. So multicellular beings are utopian aggregates of cells all cooperating to promote the chances of their clonally related sex cells. Well, not always. The cellular slime moulds are a case in point.
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Take a microscope to damp autumnal leaf litter and there you can find certain amoeboid cells grubbing for bacteria. But when nutrients become depleted, one cell sends out a chemical call to initiate the aggregation of the local flock. This aggregate becomes a multicellular mass, a motile slug-like being. When the slug has migrated to the surface, it changes into a delicate arboreal structure, reaching out from the decaying leaf mass so as best to ensure the dispersion of the tip-borne spores.

The key difference between them and us is that, in slime moulds, the cells that make up the body are not necessarily derivatives of the same initial cell. This lack of perfect genetic identity defines the central problem of the slime mould. For a cell within the slug, it is of critical importance whether it makes it into the spore or not. If it does, it gets the chance to genetically live another day in valleys greener. A cell not in the spore, however, is at a genetic dead-end. If the spore cells are not relatives, why would cells be part of the supporting cast? For a cell in the slug mass to commit to a dead-end future is as great an act of altruism as you will find anywhere. Why do they do it?

The answer comes back to who is in the spore. The cellular slime moulds go some way to try and ensure that only related cells can join their multicellular party. The molecular mechanisms by which they achieve this have only recently been unveiled. They employ proteins that participate in both cell adhesion and signalling. Importantly, the proteins show many differences between strains from the same species, so employing the rule that you should only aggregate with cells with the same version ensures the aggregates are largely kin groups. But this is never guaranteed. Sometimes, as John Tyler Bonner, the grand old man of slime mould research, notes, things don’t go to plan. There are “cheats”. These cheats will join unrelated cells, refuse to be supporters and force themselves to be spore: what in the business world might be considered an aggressive takeover. Interestingly, as Bonner relates in The Social Amoebae, a colony made up just of cheats can be rather well-behaved and produce both spore and support.

The humble cellular slime mould thus presents a model system for understanding how conflicts are resolved and how and when altruism pays. Can we then, from an understanding of when potential conflicting interests are or are not likely, understand the behaviour of the slug and its constituent cells? It is a pity that Bonner doesn’t delve into this issue in much detail, but we can speculate. Compare, for example, the problem of how a slug turns around, with the problem of attraction to heat and light.

To investigate how slugs go in reverse, Bonner relates how researchers have studied what happens when a slug slimes its way up a cul-de-sac so narrow that the only way out is to retreat the way it came in. This might be accomplished by instructing the tail end to become the head end and so move backwards. In practice, the answer is rather more baroque: the cells in the head migrate all the way to the rear, making the rear the head. It is not immediately obvious why this would be the optimal solution.

When moving towards light and heat, by contrast, the slugs show the most exquisite perfection. Sometimes, we learn, a slug prefers to move towards the warmth. Remarkably, a difference of just 0.0005°C between the two sides of a small slug is a sufficient cue. Even though they lack eyes, the slugs also move towards the light. Arrive in the lab in the morning and, like lavender desperate for the rays of the sun, they are all inclined to the window. Incredibly, just a minuscule spot of low-intensity light is enough to draw the slugs’ attention. How such feats of sensitivity are achieved is unknown. Why they might be so sensitive is easier to gauge. The important process for the slug is probably getting out from under the leaf litter, so the spores are delivered at the surface. Moving towards light is a good cue for this. Moving towards heat is less obvious. During the day this would typically send the slug towards the surface. But at night the soil retains its heat and the temperature gradient is reversed. Interestingly, however, if the heat experiment takes place when it is relatively cold (mimicking nocturnal conditions), the slugs’ preferences change: now they migrate away from warmth. As Bonner observes, day or night their temperature preferences drive them to the surface.

Can we, however, understand why the slug is so perfect in orienting to heat, but comes to a strange solution for turning around? I would conjecture that, as the spore cells will all be derived from the end that functions as the head, when it comes to turning around, the head cells have everything to lose if they simply instruct the tail to take over control. By contrast, it is in the best interests of all cells in the slug to make sure the spores disperse, so here they can all agree to reach for the skies. The head cells maintaining their hold on their reproductive future while turning around represents an alternative solution, a sort of benign dictatorship. If you ask why the tail cells don’t try and take the opportunity to become head cells, and hence become the future reproductives, the answer is not that this isn’t in their best interests, but rather that they are not given the option. The evolutionary biology of this class of solution – for want of a better term, “power” – is one waiting to be written.

How are decisions made, such as which cells become spores, or how do they become part of the slug-mass in the first place? Recounting delightfully simple experiments, Bonner details what we know about the communication between cells and how slugs develop. Given how much we still don’t know about slime mould biology, it is no surprise that he raises more questions than he answers. However, Bonner’s repeated emphasis of the unknowns is, I suspect, quite deliberate. This small book is an attempt to put down for posterity his enthusiasm and knowledge. He is here to hand over the baton, and hope that somewhere there are interested young biologists struck by the beauty of the unanswered simple questions about beautiful, apparently simple organisms.

In his search for someone to carry on the slime mould’s cause, I hope he succeeds, but have doubts. In the final chapter of The Social Amoebae, a view to the future of slime mould research, it is strikingly peculiar that nowhere does Bonner mention the fact that his beloved species is one of few organisms to have had all of its DNA, its genome, sequenced. Maybe this was because such genomic biology could not be more antithetical to the tradition exemplified by Bonner himself. This new genomic science is high on data, but often light on the questions. Discovery via high-throughput data generation is now the order of the day, however, and it looks set to soak up the big research money for a while yet. But with this approach, carefully considered hypotheses, simple elegant experiments and a feel for the organism tend to be lost by the wayside. The old-school classical biologists, such as Bonner, who really understand their organisms may well, like the slime mould’s supporting cells, find themselves without a future.



John Tyler Bonner
THE SOCIAL AMOEBAE
The biology of cellular slime molds
144pp. Princeton University Press. $19.95;distributed in the UK by Wiley. £13.95.
978 0 691 13939 5




Laurence D. Hurst is Professor of Evolutionary Genetics at the University of Bath.