In the natural world, cooperative interactions evolve not as expressions of altruism, but as careful “negotiations” between interacting species. Each player may benefit from the relationship, but each stands to benefit from trying to cheat the other. In this month’s issue of The American Naturalist, we see a prime example: mutualistic ants sterilize their host plants [$-a] to get the most out of the interaction.
The ant species Allomerus octoarticulatus is part of a classic protection mutualism with the tropical tree Cordia nodosa, in which the plant grows structures called domatia that provide shelter for a colony of ants, and nutrient rich “food bodies” for the ants to feed on. The ants, in turn, patrol the plant and drive off herbivores. This mutually beneficial relationship also sets up a conflict of interest. The tree must divide its resources between providing food and shelter for its resident ant colony — growing new domatia and fruiting bodies — and its own reproductive efforts — growing flowers and fruit. The ants, naturally, would prefer for the host tree to spend as much energy as possible on them.
Indeed, Allomerus octoarticulatus has been observed killing the flowers of its host trees. This is what led the new paper’s author, Megan Frederickson, to conduct a simple experiment on C. nodosa, asking whether such pruning prompts the tree to grow more domatia. She experimentally removed flowers from trees occupied by a species of ants that don’t engage in flower pruning to see if pruned trees grew more domatia — and pruned trees grew more domatia over the course of four months than trees that were allowed to flower and produce fruit.
Ant-hosting plants need not be totally subject to the whims of their protectors, however — this kind of regulation works both ways. A study published last year in Science found that ant-hosting Acacia trees cut back on support for their resident ant colonies [$-a] when herbivores are removed and ant protection is no longer needed. (I wrote about this study back when it was released.) It seems likely that flower-pruning ants are exerting strong selection on Cordia nodosa to circumvent this behavior — a new tree variant that can overcome pruning, or make life uncomfortable for pruning ants, should have a large selective advantage.
In the absence of such a mutation, as Frederickson points out, Allomerus octoarticulatus is creating a tragedy of the commons by reducing the long-term viability of its host tree’s populations in exchange for the short-term benefit of more living space. As it stands, Cordia nodosa can only reproduce when it hosts non-pruning ant species, which are a minority in the populations Frederickson studied. Only time, and further study, can determine whether this mutualism might break down altogether.
References
Frederickson, M. (2009). Conflict over reproduction in an ant-plant symbiosis: Why Allomerus octoarticulatus ants sterilize Cordia nodosa trees. The American Naturalist, 173 (5), 675-81 DOI: 10.1086/597608
Palmer, T., Stanton, M., Young, T., Goheen, J., Pringle, R., & Karban, R. (2008). Breakdown of an ant-plant mutualism follows the loss of large herbivores from an African savanna Science, 319 (5860), 192-5 DOI: 10.1126/science.1151579
Great post. However, you should be careful to distinguish interspecies mutualism from intraspecies cooperation. There are multiple examples of cooperation within species that don’t fall into the category you’re talking about. For example see Superorganisms and Group Selection.
Well, I think the major difference between interspecies mutualisms and intraspecific cooperation is that there’s no way relatedness can stabilize interspecies interactions. In that sense, it’s actually quite a bit like the multi-queen ant colonies you discuss in that very interesting post.
I’d imagine, then, that “group selection” for this ant-plant system could play out over a metapopulation of all the species involved, with populations going extinct when the cheater ants take over, and non-cheaters recolonizing those populations. The stability of the mutualism then depends on how frequently ants move between plant populations (and cheaters invade) and the fitness benefits experienced by populations that don’t have cheaters.
So maybe most interspecific mutualisms are, like the stable multi-queen colonies, the ones that have managed to survive over the long term. Thanks for pointing to that — I didn’t realize there were good cases of ant colonies remaining coherent without relatedness. It seems to me like a good conceptual link between relatedness-driven “altruism” within family groups and mutually beneficial interactions between different species.
You’re in the carnival:
http://quichemoraine.com/2009/05/berry-go-round-16/
Thanks, Greg – I’m glad to be included!
I enjoyed learning about this. It’s a new topic for me.
Liz at Yips and Howls
“In the absence of such a mutation, as Frederickson points out, Allomerus octoarticulatus is creating a tragedy of the commons … Only time, and further study, can determine whether this mutualism might break down altogether “
A little Cassandra, don’t you think, J-bone?
In fact there are many examples of mutualistic interactions in which one player manipulates the other to invest more in vegetative growth, and less in reproduction. Among ant/plant interactions it is actually quite common to see ants removing flowers, even when herbivores are note experimentally excluded.
Likewise, the much trumpeted leaf-cutter ant / fungus mutualism is likely a case of reduced antagonism. It is known that the fungi will occasionally produce a mushroom, which the ants quickly and judiciously chop down.
This phenomenon, known as “parasitic castration” is explored in actually quite common, and the evolutionary dynamics of parasitic castration are explored in detail in: Hall, S et al. 2007. Parasitic castration: a perspective from a model of dynamic energy budgets. Integrative and Comparative Biology 47(2):295-309
Chris – OK, so that was maybe a little over the top. The data set presented doesn’t really give us a good handle on the effects of ant species and behavior on individual trees’ lifetime fitness — just growth over a single season. And lifetime fitness is what matters, of course. I think, if my skimming is correct, that’s the takeaway point of the paper you cite (which looks to be free online for interested parties).