Perspective: Virulence

Abstract

Why do parasites harm their hosts? Intuition suggests that parasites should evolve to be benign whenever the host is needed for transmission. Yet a growing theoretical literature offers several models to explain why natural selection may favor virulent parasites over avirulent ones. This perspective first organizes these models into a simple framework and then evaluates the empirical evidence for and against the models. There is relatively scant evidence to support any of the models rigorously, and indeed, there are only a few unequivocal observations of virulence actually evolving in parasite populations. These shortcomings are surmountable, however, and empirical models of host-parasite interactions have been developed for many kinds of pathogens so that the relevant data could be acquired in the near future.

A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum

“…The vertical transmission treatment maximizes retention of mutualistic symbionts, since symbiont and host reproduction are directly tied. However, the horizontal transmission treatment should favour highly infectious symbionts potentially to the detriment of the host (Fine 1975;Ewald 1983;Bull 1994). Both treatments were replicated threefold, and two rounds of experimental transmission followed initial infection, with seven weeks between transmission rounds (figure 2).…”

“…Virulence theory, developed to study pathogen evolution, suggests that horizontal transmission promotes the evolution of harmful symbionts. There are two main predictions: (i) horizontal transmission allows symbionts to adopt selfish strategies such as appropriating resources from their current hosts before moving on to new hosts (Fine 1975;Ewald 1983;Bull 1994); and (ii) under horizontal transmission, unrelated symbionts can infect the same host, compete for host resources and harm the host in the process (Frank 1994(Frank , 1996a. Paradoxically, horizontally transmitted mutualists are common in nature, including algal symbionts of marine invertebrates (Trench 1993), mammalian gut-symbionts (Savage 1977), nitrogen-fixing bacteria in plant roots (Sprent et al 1987) and bioluminescent bacteria in fish and squids (Ruby 1996).…”

“…However, it is unclear whether these symbionts invariably offer a net benefit to hosts (Douglas & Smith 1983;Douglas 1995Douglas , 1998Muller-Parker & Davy 2001), or if they can evolve to parasitize their hosts. Numerous cnidarian hosts acquire symbiotic algae infectiously at each sexual generation (Fadlallah 1983), and theory suggests that such horizontal transmission selects for symbiont virulence (Fine 1975;Ewald 1983;Bull 1994).…”

Free-living pathogens: Life-history constraints and strain competition

“…Direct-contact pathogens are transmitted from an infectious to a susceptible host before the former recovers or dies, since the pathogen rapidly deteriorates outside host tissues. Virulence, the increase in host mortality due to infection (Bull, 1994;Ewald, 1994), may depend functionally on the rate of infection transmission. A pathogen's within-host replication rate should increase as it accelerates consumption of host resources.…”

Epidemiological consequences of a pathogen having both virulent and avirulent modes of transmission: the case of rabbit haemorrhagic disease virus

“…Theoretical work has shown how pathogen virulence can be adaptive, when it occurs as the result of a trade-off between the transmissibility of the pathogen and the lifetime of the infected host [35]. However, highly virulent pathogens are prone to local extinction, and there are a number of strategies for persistence.…”