The socio-economic challenges of managing pathogen evolution in agriculture.

Genetic resistance forms the foundation of infectious disease management in crops. However, rapid pathogen evolution is causing the breakdown of resistance and threatening disease control. Recent research efforts have identified strategies for resistance gene deployment that aim to disrupt pathogen adaptation and prevent breakdown. To date, there has been limited practical uptake of such strategies. In this paper, we focus on the socio-economic challenges associated with translating applied evolutionary research into scientifically informed management strategies to control pathogen adaptation. We develop a conceptual framework for the economic valuation of resistance and demonstrate that in addition to various direct benefits, resistance delivers considerable indirect and non-market value to farmers and society. Incentives for stakeholders to engage in stewardship strategies are complicated by the uncertain timeframes associated with evolutionary processes, difficulties in assigning ownership rights to genetic resources and lack of governance. These interacting biological, socio-economic and institutional complexities suggest that resistance breakdown should be viewed as a wicked problem, with often conflicting imperatives among stakeholders and no simple cause or solution. Promoting the uptake of scientific research outcomes that address complex issues in sustainable crop disease management will require a mix of education, incentives, legislation and social change. This article is part of the theme issue 'Infectious disease ecology and evolution in a changing world'.

Variation in infectivity and aggressiveness in space and time in wild host-pathogen systems: causes and consequences.

Variation in host resistance and in the ability of pathogens to infect and grow (i.e. pathogenicity) is important as it provides the raw material for antagonistic (co)evolution and therefore underlies risks of disease spread, disease evolution and host shifts. Moreover, the distribution of this variation in space and time may inform us about the mode of coevolutionary selection (arms race vs. fluctuating selection dynamics) and the relative roles of G × G interactions, gene flow, selection and genetic drift in shaping coevolutionary processes. Although variation in host resistance has recently been reviewed, little is known about overall patterns in the frequency and scale of variation in pathogenicity, particularly in natural systems. Using 48 studies from 30 distinct host-pathogen systems, this review demonstrates that variation in pathogenicity is ubiquitous across multiple spatial and temporal scales. Quantitative analysis of a subset of extensively studied plant-pathogen systems shows that the magnitude of within-population variation in pathogenicity is large relative to among-population variation and that the distribution of pathogenicity partly mirrors the distribution of host resistance. At least part of the variation in pathogenicity found at a given spatial scale is adaptive, as evidenced by studies that have examined local adaptation at scales ranging from single hosts through metapopulations to entire continents and - to a lesser extent - by comparisons of pathogenicity with neutral genetic variation. Together, these results support coevolutionary selection through fluctuating selection dynamics. We end by outlining several promising directions for future research.

Contrasting impacts of pollen and seed dispersal on spatial genetic structure in the bird-pollinated Banksia hookeriana.

In plants, pollen- and seed-dispersal distributions are characteristically leptokurtic, with significant consequences for spatial genetic structure and nearest-neighbour mating. However, most studies to date have been on wind- or insect-pollinated species. Here, we assigned paternity to quantify effective pollen dispersal over 9 years of mating, contrasted this to seed dispersal and examined their effects on fine-scale spatial genetic structure, within the bird-pollinated shrub Banksia hookeriana (Proteaceae). We used 163 polymorphic amplified fragment length polymorphism markers to assess genetic structure and pollen dispersal in a spatially discrete population of 112 plants covering 0.56 ha. Spatial autocorrelation analysis detected spatial genetic structure in the smallest distance class of 0-5 m (r=0.025), with no significant structure beyond 8 m. Experimentally quantified seed-dispersal distances for 337 seedlings showed a leptokurtic distribution around a median of 5 m, reaching a distance of 36 m. In marked contrast, patterns of pollen dispersal for 274 seeds departed strikingly from typical near-neighbour pollination, with a distribution largely corresponding to the spatial distribution of plants. We found very high multiple paternity, very low correlated paternity and an equal probability of siring for the 50 closest potential mates. Extensive pollen carryover was demonstrated by multiple siring in 83 of 86 (96.5%) two-seeded fruits. Highly mobile nectar-feeding birds facilitate this promiscuity through observed movements that were effectively random. As the incidence of bird-pollination is markedly greater in the Southwest Australian Floristic Region than elsewhere, our results have broad and novel significance for the evolution and conservation for many species in Gondwanan lineages.