Pondering Pikaia: Fig Tree Friends and Foes

The natural world is full of examples of pairs of species that are dependent upon each other for survival, co-existing due to mutualistic interactions, often as a result of co-evolution. The case studies are numerous: clownfish and anemones, oxpeckers and rhinos, and the yucca and yucca moth (the existence of the moth was predicted by Darwin in his commentary on the long floral tube of the yucca flowers, before the insect had actually been discovered!).

Although these examples of interdependent species make for nice case studies in symbiosis, they also present a conundrum for scientists: what prevents cheating? How does evolution lead to an equilibrium state, in which one species does not take complete advantage of the other, as we see in parasitic relationships? This week PLoS has a fascinating paper out that describes how the well-known mutualism between fig trees (Ficus rubiginosa) and pollinating fig wasps (Agaonidae, which function as pollinators, see an excellent diagram fo the life cycle here) is stabilized by a third species, a different species of fig wasp that does make its living as a parasite, not a pollinator.

In order to understand how the interdependence between fig trees and pollinating wasps is stabilized by the parasites, we need to know the basic dynamics of the relationship. The technical word for the inflorescences that produce figs is "syconia," and this is where the action takes place. Pollinating wasps enter the syconia to oviposit their eggs, and in the process they pick up gametes from the flower that are later transferred to a different tree. Thus, trees benefit from pollination, and wasps benefit from a safe place to put their eggs. The oviposition creates a gall in the syconia and costs the tree a fruit, but that is compensated by the many fruits that can be produced later after gametes are carried by the wasps.

It seems nice and simple, but, as with most things in nature, there is more complexity here than first meets the eye. The floral styles of ovules within the syconia can vary widely in length, and pollinating wasps have been shown to preferentially lay their eggs in flowers with short styles. The question is: why? What is it about flowers with shorter styles that make them the favorites of pollinating wasps?

The answer: location, location, location. Ovules with shorter styles tend to develop within the inner part of the syconia, indicating that it could be relative position, not only relative length, that is the key factor. There have been several different hypotheses suggested to explain the phenomenon: pollinators may start filling ovules at the inside and simply run out of eggs before reaching the outer ovules, their ovipositors could be too short for the flowers with longer styles, or outer ovules may have special biochemical defenses. None of these ideas have been strongly supported, however.

It appears that a third species in this system is actually important for determining the relative fitness of eggs deposited in inner versus outer ovules. There are nonpollinating, parasitic wasp species that also make their livings on fig trees. These beasties also lay their eggs in the tree's syconia, but instead of finding their own egg sites they insert their ovipositors into ovules that already contain the eggs/larvae of pollinating wasps, taking advantage of a ready-made gall and eliminating the former inhabitant.

Dunn et al (2008) show that a pollinator's risk of having its gall hijacked decreases substantially if they select inner versus outer ovules. Ovules nearest the exterior had an 80% chance of being parasitized, while those in the innermost ovule had virtually no risk (0%). One key finding is that parasitic larva DO occur in the outer ovules, which means that the pollinating species had to have deposited eggs there first, showing that they are indeed capable of planting their seeds in ovules, it is just a bad decision to do so. This is counter to some of the alternate hypotheses, mentioned above, that work on the idea that pollinators are for some reason incapable of putting eggs in the outer ovules.

So, pollinating wasps put their eggs in figs, they put them as close to the center as they can so that the parasitic species can't take them over. It makes perfect sense, and doesn't seem that sensational. What is very significant about this case, however, is that it is an example of how a mutualism is actually facilitated by a third parasitic species. The parasite wasp can be seen as a "bully" that forces the pollinating wasp to avoid ovipositing in outer ovules. This limitation prevents a female wasp from filling every ovule with eggs, and decreases the number of seeds that the tree sacrifices in order to use the wasp as a pollinator.

One thing that came to my mind, that wasn't explicitly directly addressed in the paper: Could we also see this as a case of two positive mutualisms, one between the tree and the pollinator in addition to the tree and the parasite species that keeps the pollinator in check? The parasite is what appears to help the pollinator from "cheating" and becoming another parasite on the tree, so being an enemy of a potential enemy makes it a benefit to the tree. When you include the parasitic relationship between the two wasp species, that would make for a triad of interactions, none of which could remain stable without the third. Too bad these are fig wasps instead of paper wasps, I could have made a great pun about "paper, wasp, scissors". . .