The stable association of viruses with their natural host places specific constraints on the nature of viral disease and mode of persistence

As noted previously, viruses are maintained by active rounds of infection somewhere in their reservoir. We have seen that a virus infection leading to immunity to reinfection will lead to virus extinction in a small population once the pool of susceptible individuals is exhausted. Also, even in a large reservoir, if the virus infection directly or indirectly leads to death of a large enough number of individuals, the host population of the reservoir will crash and, in extreme cases, may become extinct. Clearly, a virus, which can only replicate within that population, will also become extinct. These limitations, which can be described with precision using the mathematics of population biology and epidemiology, lead to a number of evolutionary constraints on the dynamics of the virus—host interaction. Viruses whose infection leads to an acute disease followed by clearing and immunity will need a large host population while the outcome of the disease cannot be too lethal or the virus cannot be maintained. However, if infection results in mild or inapparent symptoms, there still must be efficient spread. This latter pattern of virus infection is a common feature of viruses with animal reservoirs that contain large populations such as flocks of migratory birds or herds of ungulates. Since the agricultural/ urban revolution starting about 10,000 years ago, which engendered rapid increases in our population, urbanized human populations fit this criteria also.

The early history of humans, however, was not one of large sedentary populations. Rather, our ancestors lived in small, nomadic groups organized along familial lines. This organization is similar in broad outline to that of predators such as wolves and large cats. In such a population no virus that is cleared with resulting immunity can persist; therefore, only a virus that can establish a persistent infection of its host with little or no diminution of the host's ability to survive and propagate can persist. Further, this persistence must allow for infectious virus to be present at opportune moments for infection of new, susceptible individuals (i.e., infants and occasional adults encountered from other groups). A number of viruses have replication strategies and genetic capacities to establish such infections, and it is striking that genetic analysis of such viruses demonstrates ancient associations with humans.

These two basic, nonexclusive strategies of virus replication are shown in Fig. 4.1. Of course, not all viruses are constrained by their narrow host range to infect just one species or type of host. Some, notably a number of viruses using RNA as their genetic material, have a broad host range and can readily jump from one species of host to another. With such a virus, the constraints on the mortality of the disease caused in the novel or ancillary target population do not exist. It is not particularly surprising, then, that mortality rates of some diseases caused by zoonotic viruses are quite high.

Other factors further complicate the simple patterns of virus infection and persistence outlined above. A notable one is that if the period of time between the initial infection and the

Fig. 4.1 Virus maintenance in small and large populations. (a) In a small population virus infection can only occur when there is an immunologically naïve individual available. This requires a virus within such a population to be able to maintain itself in an infectious state in individuals long after they have been infected. A favored mode of infection would be from parent to child. Clearly, high mortality rates or severe disease symptoms would be selected against. (b) In a large population, there will be a large number of susceptible individuals appearing at the same time. This can result in local episodic infections of such individuals. The large size of the host population insures that some virus is available from actively infected adults at all times. While persistence is not excluded, it need not be strongly selected for, especially if the course of the acute phase of the disease is relatively long compared to the generation time of the population.

Parent or elder persistent virus infection with episodic shedding

Parent or elder persistent virus infection with episodic shedding

Spreading virus to next generation and rarely to other small groups via chance encounters

Virus can persist in subgroup in large population and spread sporadically to other subgroups

appearance of symptoms (the incubation period) are longer than the generation time of the host, constraints on mortality are lost. This is the case for rabies, which exhibits essentially a 100% mortality rate in infected carnivores — its natural host, but its very long incubation period allows reproduction even after infection. The life span of humans is so long that this might not seem to be a major factor in maintaining virus infections with high mortality rates, but the association between certain persistent human virus infections and the very much later appearance of tumors and immunopathologies are a consequence of a long incubation period between initial infection and ultimate pathology.

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