Acute and persistent viral life strategies and their relationship to emerging diseases.

Most virologists would accept the concept that particular viruses often appear to have either acute or persistent patterns of host infection. The polyomaviruses of mammals, for example, uniformly establish persistent infections of a specific host. In contrast, it has recently become clear that avian polyomaviruses infect a broad array of bird species in an acute pattern (Lafferty et al., 1999; Phalen et al., 1999; Johne and Muller, 1998). In this review, we develop the proposal that these two infection patterns define two life strategies of viruses with distinct evolutionary ecologies and consider the consequences on viral fitness and the ecological and evolutionary relationships. We suggest that persistent host-specific viral agents are the origin of emerging acute epidemic disease following adaptation of that virus to new host species. The concept of life strategy for a species was first applied in an island biogeographical context where it appeared that specific organisms were better adapted either for initial habitat colonization (r-selected) or for long-term population equilibria (K-selected) (MacArthur and Wilson, 1967). We have previously considered if specific viruses might also exist with distinct life strategies. However, since various acute viruses can be both a virgin soil epidemic (r-selected) and a childhood infection at equilibrium in the population (K-selected), these life strategies cannot be applied to individual viral species (Villarreal, 1999). Yet viruses do appear to have distinct patterns of acute and persistent host infection. Viral persistence has been considered with respect to sources of epidemic disease (Mahy, 1985; Domingo et al., 1998; Holland, 1996; Oldstone, 1998a). However, the term persistence can often include persistence of viral agents in host populations or in the environment [better termed viral durability (Cooper, 1985)]. To elucidate a more specific relationship between the virus and individual host, in this review we limit the definition of persistence to only apply to viral persistence in an individual host. The acute viral life strategy is a transient pattern of host infection in which the host immune response will eliminate or prevent the same virus infection from continued reproduction in that same host. Thus, these viruses must find a new host during the limited period of virus reproduction in order to continue their infectious cycle. This familiar life strategy applies to many human viral infections that are responsible for epidemic disease (smallpox, measles, poliovirus, influenza virus, rhinoviruses). These acute viruses have a high dependence on host population structure as described by the apparently accurate mathematical models that resemble predator– prey dynamics in which the viruses act as predators on their host prey (MacArthur and Wilson, 1967; Anderson and May, 1991). Several distinct characteristics apply to acute viruses. They are often disease associated, show high mutation rates (in RNA viruses), can exist in genetically diverse quasi-species (Domingo and Holland, 1997; Domingo et al., 1998; Domingo, 1998), and frequently appear able to replicate in more than one species. Acute viruses tend not to show cospeciation (phylogenetic congruence) with their hosts and are more frequently found in hosts that exist as congregational (herd, flock) populations. It has previously been postulated that acute and virulent viral disease must represent a newly infecting virus for the host since viral-induced host death will negatively affect host fitness and should consequently limit host availability (Dubos, 1965; Burnet and White, 1972). Therefore, older, more established viruses may be more benign to their host. More recent theoretical considerations, however, challenge this view (Ewald, 1994; Frank, 1996; Lipsitch et al., 1996). Highly virulent viral infections of large host populations do not seem to generally evolve from the acute to 1 To whom correspondence should be addressed. Fax: (949) 8248551. E-mail: lpvillar@uci.edu. Virology 272, 1–6 (2000) doi:10.1006/viro.2000. 0381, available online at http://www.idealibrary. com on