Using multispecies evolutionary history to test hypotheses of community assembly

Insect herbivores and their insect natural enemies are the most species rich groups of terrestrial animals on Earth, making up between 33 and 50% of all species. They provide a wide range of ecosystem services, including pest control and pollination, and provide food for other components of animal diversity. Understanding how these communities come into being and persist through time is central to long term management of biodiversity and of the ecosystem services they provide. This project examined the evolution of a particular herbivore/enemy community – oak feeding gallwasp herbivores and their parasitoid wasps. This group is rich enough to represent other natural groups (there are around 1000 oak gallwasps across the Northern Hemisphere worldwide, and the same number of enemies), and has long been seen as convenient to study because the enemies are thought only to attack oak gallwasps – so the system can be studied in isolation. This project used DNA sequence datasets to address 3 general questions about the evolution of animal communities, provided here with summary answers. All of the aims of the project were achieved, leading to ongoing international collaborations and multiple publications.

This project set out to examine how biological communities (sets of animals and plants living in a given region) come to exist there. Do such communities share a long history, in which case they are likely to be very highly adapted to each other? Or have they come together in the recent past, such that, if damaged, the community could probably be restored? These questions are crucial ones given ongoing disruption of natural habitats through human activity and climate change. Our results - based on detailed study of one example community involving plants, plant-feeding insects, and their predators - suggest that at least some communities will often share extensive joint history, and be hard to restore if species are completely lost,

1. How have gallwasps and their enemies diversified across the Earth?
Our research shows that gallwasps spread across the Earth from an origin in Eastern Asia – where we have recently discovered many new and distantly related gallwasps. From Asia they spread westwards in Europe from around 10 million years ago, and eastwards across the Bering Straits into America (perhaps as long as 17 million years ago).
2. How often do communities of herbivores and their enemies shift (in evolutionary terms) between different groups of plants?
Early in gallwasp diversification, lineages became specialised to particular groups of oaks and their relatives, with very few shifts between host groups thereafter. Their enemies, however, are far more able to transfer between gallwasp hosts on different plant groups: we found shifts in both directions between oaks and roses, and (in Europe) between oaks and chestnut. These latter shifts are important, because the chestnut gallwasp is a major invasive pest in the northern mediterranean, and parasitoids that normally attack oak gallwasps are contributing to the development of biological control. More generally, we argue that ‘leakiness’ of parasitoid communities may contribute to their longer term survival in the face of metapopulation and larger scale variation in host abundance.
3. How do gallwasp communities develop locally? Do species in the different trophic levels share a common origin? Did herbivores and enemies spread together, or did herbivores sometimes escape their enemies?
This extension of question 1 looked at the development of communities in Europe and Asia minor, and compared the population histories of 31 species – 12 gallwasps and 19 parasitoids. These species are now all found right across Europe, and we used DNA sequence data to look at the extent to which herbivores and their enemies spread together, or separately. We found that most of the species have a shared origin in the east (in Turkey and/or Iran), and spread across Europe in the last 2 million years. The herbivores often escaped their enemies for periods of many thousands of years during westwards range expansion, though their enemies ultimately caught up with them once more – most recently over the last 10-20 thousand years in Spain. This means that although communities in the east and west share most of the same gallwasp and enemy species, they have very different histories; in the east, herbivores and enemies have evolved in each others unbroken company, while in the west the associations have been fragmented and sometimes only recently restored in evolutionary terms. The evolutionary interactions between herbivores and enemies – most often viewed in terms of a ‘tit for tat’ arms race – can thus be very different between locations, and different populations of the same species may have faced quite different selective pressures. Population history must be incorporated into understanding of community structure.
During the progress of this research, it has become clear that many of the species recognised by taxonomists in fact comprise multiple ‘cryptic’ species, which we can only distinguish by using DNA sequence information. One of the outputs of this project has been the development of a ‘DNA barcoding’ resource for oak gallwasp communities. Though oak gallwasps may seem as esoteric choice of community, they share many characteristics – in terms of distribution, species richness, and natural enemy community structure – with many other herbivore groups, including many economically important species. It is likely that the patterns we show for them will apply much more widely in herbivore-enemy communities.