Tracing the role of human civilization in the globalization of plant pathogens

Abstract

Co-evolution between plants and parasites, including herbivores and pathogens, has arguably generated much of Earth's biological diversity. Within an ecosystem, co-evolution of plants and pathogens is a stepwise reciprocal evolutionary interaction: epidemics result in intense selection pressures on both host and pathogen populations, ultimately allowing long-term persistence and ecosystem stability. Historically, plants and pathogens evolved in unique regional assemblages, largely isolated from other assemblages by geographical barriers. When barriers are broken, non-indigenous pathogenic organisms are introduced into new environments, potentially finding suitable hosts lacking resistance genes and environments favouring pathogenic behaviour; this process may result in epidemics of newly emerging diseases. Biological invasions are tightly linked to human activities and have been a constant feature throughout human history. Several pathways enable pathogens to enter new environments, the great majority being human mediated. The fossil record provides evidence that diseases commonly affected plants some 250 million years ago (Dark & Gent, 2001). The recurrence of wheat rust outbreaks is reported by Roman authors such as Cicero, Varro and Columella (2100-1950 BP). Rust outbreaks were so feared that there was a god/goddess of rust (Robigus/Robigine) to whom processions, sacrifices and feasts were dedicated in order to prevent crop destruction. During the last 200 years the incidence of plant diseases has increased exponentially in terms of both numbers and severity (Santini et al, 2013). Alien pathogen introductions can lead to novel host-pathogen associations or novel pathogen-pathogen combinations, with no previous co-evolutionary history. Why are so many invasive plant pathogens now appearing? The aim of this paper is to increase understanding of the means of introduction and spread of these pathogens, which, as with most invasive species, can be traced to human behaviour, societal development, technological change, and geopolitical trends. We believe that reviewing historical developments enhances our ability to anticipate future developments.