Conflict resolution in mutualisms.

Lead Research Organisation: University of Reading
Department Name: Sch of Biological Sciences

Abstract

Many organisms are involved in intimate associations with other species. In general the smaller partner (symbiont) lives partly in or on the larger partner (host). Symbioses can be beneficial to both partners, in which case they are called mutualisms, or can involve one partner (the parasite) inflicting harm on the other (host). Even when both partners appear to gain from the association, they do not always have the same evolutionary interests. There is no hard and fast border between parasitism and mutualism and it is important to understand what factors favour positive or negative effects of the symbiont on the host. This is especially so if the symbiont is only parasitic under certain circumstances, as in many microbial infections of animals. More generally, mutualism is of immense importance in biology, both in the short and long term. For example, their association with rhizobial bacteria allows bean plants access to nitrogen. Mutualism can also lead to major evolutionary events and the two major genetic components of our cells (nucleus and mitochondria) had their origins in an ancient mutualism. Despite the importance of mutualism, there is no general theory that explains when we should expect a mutualistic outcome, or how the mutualists resolve their conflicts. However, there is increasing evidence that hosts can limit the parasitic tendencies of symbionts by controlling their access to key host resources and also influencing the way in which different individual symbionts have to compete with each other for access to host resources. This type of explanation could be applicable in a wide variety of cases including plants and pollinators, plants and nitrogen-fixing bacteria, and even some human diseases. This project will investigate how hosts control their symbionts using a model system involving fig trees and their pollinating wasps. This is a mutualistic interaction, but one with clear conflicts. Specifically, while figs need wasps to pollinate their flowers, the wasp larvae eat some of the fig seeds. The fig needs to manage the wasps so that they do not lay eggs in all the seeds. Figs may manage wasps by altering the quality and architecture of the fig flowers so that some are more desirable sites for wasp to lay eggs. This may be because some flowers are better places for wasp larvae to develop, or because some flowers are easier for wasps to lay eggs into, or both. In theory, the wasps' preference for certain flowers, plus the fact that they waste time rejecting flowers that they deem unsuitable, or flowers in which other wasps have laid eggs (only one egg can develop per flower), can prevent the wasps from exploiting too many of the seeds and allow the mutualism to persist. We will test this idea by making detailed studies of five pairs of figs and their pollinators, choosing the species to reflect the great differences in biology seen across the over 750 species of figs in the world. We will video and analyse the flower searching and egg-laying behaviour of wasps and also assess whether certain flowers give rise to better (bigger) wasp offspring. We will use the data to test the theoretical model for each species. We will also estimate just how much conflict there is between the fig and wasp partners in each case, by measuring the average number of wasps entering a fig, the average number of eggs per wasp, and the average number of flowers that these eggs could potentially exploit. In addition, we will investigate whether some fig species use extra mechanisms (such as rapid flower wilting) beyond those mentioned above to stop wasps laying too many eggs. Overall, the project will be a detailed investigation of how diverse fig species stop their pollinators from destroying all their seeds (thus allowing the mutualism to persist), using a new approach that should help us to understand not only these, but perhaps most mutualisms.
 
Description Three ways by which evolution maintains cooperation in the fig-wasp mutualism.



The goal of our project was to explain how fig trees control their pollinator wasps. Fig trees are known as keystone species in tropical forests, because figs feed mammals and birds when other fruit is not available. Fruit production is of course dependent on successful pollination of fig flowers, and the only pollinators of fig flowers are tiny specialised wasps, which fly into fig inflorescences, spread pollen, lay eggs, and die. The eggs hatch into new wasps, which eat some of the developing seeds, mature, emerge, gather pollen, and fly to a new tree, completing the cycle. This intricate relationship between fig tree and fig wasp depends entirely on the wasps not laying so many eggs that their offspring eat all the seeds. But the problem is that any wasp that lays lots of eggs would be favoured by natural selection, even at the cost of driving the whole symbiosis extinct, if the entire seed crop is eaten up. We therefore looked for ways in which the fig tree can prevent wasps from evolving to lay lots of eggs.



The particular interest of the fig-wasp symbiosis is that fig trees have very long generation times compared to fig wasps, so in principle, one should expect the wasps to win the coevolutionary arms race. How can a slow-evolving tree out-evolve a fast-evolving insect? This is a particular example of a very general question in biology. How can one species win a coevolutionary arms race?



Over the course of the project, we discovered three mechanisms:



1) Insufficient wasp mothers with extra-short lifespans. If a fig does not receive enough wasps, with enough eggs, to eat all seeds, then naturally, the fig will produce seeds. We showed that this happens a lot in figs. Typically, a fig biologist will calculate that if a single wasp has enough eggs to lay in 10% of a fig's flowers, then 10 wasps should be enough to fill all flowers and eat all seeds. And if there are typically more than 10 wasps in a fig, and there are still seeds, then we have a mystery. But in fact, this is the wrong calculation. The first wasp lays its eggs in the flowers that are the fastest to oviposit in and are the most valuable. These are the flowers near the fig's hollow centre, where the wasps operate. But that means that the next wasps are pushed to lay their eggs in flowers that are further from the centre and less valuable (in part because they are more exposed to parasites that kill the wasp larvae - Dunn et al. 2008a; Al Beidh et al. 2012). So the second wasp might only be able to oviposit in 8% of flowers, the third wasps even less, and so on. Thus, in this hypothetical example, even 15 wasps might not be enough to fill a fig with eggs. Moreover, in the summer, when figs heat up, wasps die very quickly inside a fig, and this also means that even a lot of wasps might not be able to fill a fig with eggs. As it happens, these effects are enough to explain the persistence of seed production in some, perhaps many, figs (Dunn et al. 2008a,b; Wang et al. 2009, 2013).



2) Interference competition. A second mechanism is that fig wasps impede each other. The analogy is to a crowded highway. When a highway is filled with cars, traffic slows down, because drivers find it difficult to avoid interfering with each other. We did an experiment and found that when a lot of wasps enter a fig at the same time, their ability to lay eggs is greatly reduced (Wang et al. 2009, 2013), meaning, again, that many wasps with many eggs still could be unable to fill a fig with eggs.



3) Figs kill some eggs. The third mechanism is that figs seem to be able to kill some wasp eggs before the eggs hatch (Wang et al. 2013), but this only happens in the fig flowers that are far from the fig centre, and these are the flowers that are less favoured by the wasps. Normally, one might expect the wasps to be able to evolve to counter any plant defense. But if the wasps are evolved to concentrate their egg-laying on inner flowers, which are more valuable to the wasps, then there might be a trade-off that prevents the wasps from evolving adaptations to be able to survive in outer flowers. For instance, maybe wasp larvae digest seeds very quickly; this would leave them vulnerable to plant toxins in outer flowers. But if wasps were to evolve defenses against those plant toxins, then that might reduce growth rates and survivorship in the inner flowers, where most of the wasp eggs have been laid, and that would not be selected for by evolution.



The take-home messages are that it is possible for a slow-evolving species to win a co-evolutionary conflict with a fast-evolving species and that there are many ways by which a cooperative symbiosis, a mutualism, can be maintained despite strong natural selection on one side to evolve selfish cheating behaviours.
Exploitation Route The understanding of conflicts in a pollination mutualism can provide insights to mechanisms and issues that apply in other conflict / cooperation situations such as human societies and plant/microbe nitrogen-fixing partnerships in agriculture
Sectors Agriculture, Food and Drink,Environment
 
Description Early Career Fellowship
Amount £140,000 (GBP)
Organisation The Leverhulme Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 06/2009 
End 06/2011