Evolutionary Constraints on Emergence of Plant RNA Viruses

Over the recent years, agricultural activity in many regions has been compromised by a succession of devastating epidemics caused by new viruses that switched host species, or by new variants of classic viruses that acquired new virulence factors or changed their epidemiological patterns. Although viral emergence has been classically associated with ecological change or with agronomical practices that brought in contact reservoirs and crop species, it has become obvious that the picture is much more complex, and results from an evolutionary process in which the main players are the changes in ecological factors, the tremendous genetic plasticity of viruses, the several host factors required for virus replication, and a strong stochastic component. The present chapter puts emergence of RNA viruses into the framework of evolutionary genetics and reviews the basic notions necessary to understand emergence, stressing that viral emergence begins with a stochastic process that involves the transmission of a pre-existing viral strain with the right genetic background into a new host species, followed by adaptation to the new host during the early stages of infection.

accompanied by a significant increase in symptom severity (Cleaveland et al., 2007). According to the USA Center for Disease Control and Prevention, an emergent virus should meet the following definition: a disease of infectious origin whose incidence has increased within the past decades or threatens to increase in the near future. However, this definition is somewhat vague and misleading, and a virus may be classified as emerging for reasons that have little to do with the spirit of the term emerging, such as increasing awareness, the adoption of improved diagnostic tools, or the discovery of previously uncharacterized agents for already known diseases. Similarly, truly emerging viruses may not be recognized as such due to poor case reporting, or difficulties in diagnosis. Following Woolhouse and Dye (2001), a more rigorous definition of an emerging virus would be the causal agent of ‘an infectious disease whose incidence is increasing following its first introduction into a new host population or whose incidence is increasing in an existing host population as a result of long-term changes in its underlying epidemiology’. This definition implies that the virus is spreading in the host population upon its first description and it has nothing to do with changes in symptomatology. According to Woolhouse and Dye’s definition, the epidemic spread during the late 1980s and early 1990s of necrogenic strains of cucumber mosaic virus (CMV) on tomato crops in eastern Spain (Escriu et al., 2000) would hardly be considered as an emerging virus. However, it would be qualified as an emerging disease by Cleaveland’s definition. By contrast, pepino mosaic virus (PepMV), which

was first described infecting tomatoes in 1999 in The Netherlands (Van der Vlugt et al., 2000), and is now quickly spreading across Europe and beyond, should be considered as a paradigm of emerging viral infection by Woolhouse and Dye’s definition. However, I find that no definition is entirely satisfactory, and the discrepancy entirely semantic, and thus hereafter I will use a slight modification of Woolhouse and Dye’s definition that incorporates also changes in pathology. This will allow me to classify both of the above examples as emerging plant diseases. The sources of emerging viruses are different host species, the reservoirs, in which the virus is already established. Species jumps (aka spillovers) have given rise to devastating epidemics in crop species. However, there are numerous examples of species jumps that have had far less dramatic consequences (examples are cotton leaf curl virus infecting ancient cotton cultivars in India, and maize rough dwarf virus infecting maize in the Mediterranean region before the introduction of the American high-yield hybrid cultivars – see Thresh (2006) for a review) and there are even many viruses that have a long history of routinely jumping between species without triggering major epidemics (e.g. CMV). In the following sections I will go through the mechanisms and processes that are behind plant RNA virus emergence. These processes will be divided into three phases. The first phase accounts for the mechanisms and limitations for jumping the species barrier. The second phase includes the study of the evolutionary dynamics that end up with a virus well adapted to its new host. The third phase comprises the epidemiological spread of this well-adapted virus in the new host population. I will focus this review entirely on RNA viruses because of their apparent larger evolvability, the consequence of combining highly error-prone replication, large population sizes and rapid replication rates (Elena and Sanjuán 2008). For the moment, let’s reserve the discussion on whether RNA viruses are more evolvable than DNA ones for a different place, and let’s assume that the principles that drive RNA virus emergence will not be substantially different from those driving DNA virus emergence (Chapter 15). By doing so, whatever lesson may be taken from this review may help readers to understand the emergence of their favourite plant DNA virus.

Peer reviewed