What makes a specialist special? The physiology of ecological specialization in plant-fungal mutualisms

Ecological specialization is the process whereby an organism adapts to a narrower range of conditions than a generalist, and the process is central to the distribution and maintenance of global biodiversity. Yet, theory underpinning the evolution of ecological specialization has failed to i) fully consider situations where both generalist and specialist organisms form close associations with the same partner, and ii) identify the physiological mechanisms that lead to specialization in organisms that form mutually-beneficial relationships. The situation in (i) is prevalent in the widespread and globally-important mutualism that occurs between many tree roots and soil-borne 'ectomycorrhizal' fungi. Thus our understanding of the factors that drive the evolution of specialists and generalists in ectomycorrhizal symbioses is presently inadequate.

In this proposal, we will test the hypothesis that differences in resource transfer between plants and ectomycorrhizal fungi (carbon from plants to fungi, and nitrogen and phosphorus from fungi to plants) are key fitness consequence of specialization. We predict that specialist ectomycorrhizal fungi, i.e. those that often associate with just one genus of host plant) transfer more mineral nutrients to host plants for a given unit of carbon received from the host plant compared to generalists (i.e. they have a more favourable 'resource exchange rate'). We predict this efficiency in resource exchange makes them better competitors, however, we expect competitive advantage to be seen only under a limited breadth of niches. For example, such a situation may occur when specialist and generalist fungi are competing for resources from litter belonging to the 'specialist' host plant. We will also test the hypothesis that the spatial distribution of generalist and specialist ectomycorrhizal fungi on individual root systems affects acquisition of carbon from plants, and its subsequent allocation to external mycelium, and thus their ability to coexist.

To test these hypotheses, we will establish microcosms in which plants are colonised by host specialist and generalist ectomycorrhizal fungi in which the spatial distribution and scope for competition between the fungi is manipulated. We will also introduce different litter types to provide substrates that differ in suitability for the specialist. Stable and radioisotope tracers will be used to quantify resource exchange between partners and the efficiency of carbon use by ectomycorrhizal fungi relative to mineral nutrient transfer. These experiments will be complemented by field-based bioassays using seedlings inoculated with specialist and generalist ectomycorrhizal fungi, which are transplanted to environments that are deemed either favourable or unfavourable for specialists and generalists.

We aim to engage the general public through educational activities associated with the project (see Pathways to Impact). We think the general public is a crucial group to inform, especially given the general lack of awareness of the key roles fungi play in many processes. Our Pathways to Impact exploits the proximity of the Cruickshank Botanic Gardens to achieve this aim.

We also aim to engage local science secondary school teachers, who have the responsibility of enthusing at an early age the next generation of ecologists. This aim is particularly important and timely given the recent change to the national curriculum (Curriculum for Excellence). To achieve this we will liaise with professional staff very closely involved with school teacher training at the University's Natural History Centre.

The rationale for the work we propose is ostensibly quite academic in nature, in that it deals with fundamental questions about the consequences of the evolution of specialization using ectomycorrhizal trees as models to test our hypotheses. However, these consequences have important implications for a range of stakeholders. The Forestry Commission will be particularly interested in the role of ectomycorrhizal fungi in affecting biogeochemical cycles. Current environmental policies aim to both maintain and enhance biodiversity and yet reduce losses of carbon and nutrients, and it is possible for these two aims to conflict.

The Forestry Commission will also be further interested in how the presence of different types of ectomycorrhizal fungi affects tree productivity. They have a strong interest in achieving maximum crop yield and we will determine whether this is affected by varying the ectomycorrhizal fungal communities. The Forestry Commission also has a key role in maximising soil carbon storage because of the vast area of forests that they manage. Increasing carbon storage is a central part of UK legislation and out data will provide the evidence-base to develop effective management strategies that optimise carbon storage. This aim requires a better understanding of the carbon cycle more generally in forests, and a key component of our work quantifies the flux of carbon into soils, and its release as CO2.

Other stakeholders include: Scottish Natural Heritage (SNH) who will be interested because they have a statutory requirement to protect and enhance UK's biodiversity, including fungi. Our results will help demonstrate the key roles ectomycorrhizal biodiversity plays in enhancing ecosystem functioning.

Inter-agency Plant Conservation Working Group; this is a multi-agency group based in the UK aiming to develop plant conservation good practice.

Other conservation groups are also increasingly interested in the role ectomycorrhizal fungal diversity and their effects on plants (e.g. Plantlife International, Trees for Life). Indeed, there has been a recent move to strengthen the profile of fungi across the UK that has involved groups like Plant Life, British Mycological Society, and the UK Fungal Conservation Forum.

The needs of the UK Biodiversity Research Advisory Group (UK BRAG) who highlight the urgent need to understand the link between plant and microbial functional diversity.