Symbionts or genes? Integrating the evolutionary response to parasites across varying modalities of resistance.

All animals and plants are attacked by natural enemies - pathogens, parasites and predators - and the resulting mortality and morbidity drives ecological and evolutionary change. Indeed, much of animal biology is driven by natural selection to avoid or mitigate the impact of natural enemy attack, in the form of defences at the body surface to repel invaders, and defences within to clear attackers or reduce the damage caused.

Most commonly, we think of defence systems as encoded in an animal's genome. Natural selection will cause genetic variants that provide resistance to increase in frequency when attack is common, and decline if they are costly in the absence of attack. However, recent work has found that symbiotic bacteria living within the animal can also provide protection against attack. In insects, these protective symbionts are commonly passed from mother to offspring, so they behave like genetic traits. The presence of attackers will mean individuals carrying the symbiont leave more offspring, and thus natural selection increases the frequency of the symbiont.

The discovery that animal populations can evolve resistance to attack by both changes to the genome and by the spread of symbionts raises fundamental evolutionary questions. However, because the two processes have been studied in isolation, we have little understanding of how they interact and differ. To address this gap in our knowledge, we propose to study how genes and protective symbionts contribute to the evolution of resistance to parasitic wasps in laboratory populations of fruit flies.

Our first aim is to understand how different modes of protection interact within individuals and populations. If both types of variation exist, does stronger resistance evolve? Environmental factors, like temperature and food stress, have very different effects on the different modes of resistance. We will therefore test whether the environment determines which mode of resistance evolves.

We will then examine two aspects of symbiont defence that make them distinct from defence within the genome, and determine how these impact the evolution of defence.

The first distinction is that protective symbionts typically have multiple effects on their host - aside protection, they can provide nutritional benefits, alter thermal tolerance, and favour the production of daughters over sons. It is the combination of these traits that drive symbionts to spread within populations, and multiple effects thus potentially favour protective symbionts defences over genes in the genome. We will test this hypothesis by examining how sex ratio distortion shifts the balance between genes and symbionts during the evolution of resistance.

The second distinction is that protective symbiont mediated defence is an unusual trait. It is not simply 'off' or 'on', but the efficiency depends on the number of bacteria present, like an army is more effective when it contains more soldiers. The number of symbionts ('titre') can be affected by the environment, and importantly, can be transmitted between generations. A female who has many bacteria and is well defended produces daughters who likewise have many bacteria and are well defended. This unusual arrangement means that natural selection may act on the number of bacteria. Our final aim therefore is to investigate symbiont titre and the degree to which it impacts on the evolutionary response to parasite attack. Does natural selection act on titre? Do these effects last over generations? Does this process produce close tracking of resistance to the parasite threat level?

This study will be the first investigation of how the existence of these two defence modes shapes resistance evolution. The understanding gained will aid prediction of the evolutionary responses of pests and vectors to attack, which will inform our understanding of biocontrol and disease transmission by mosquitoes and other vectors.