Parasites and their Virulence





ABSTRACT

Why do some parasites kill the host they depend upon while
others coexist with their host? Two prime factors determine parasitic
virulence: the manner in which the parasite is transmitted, and the
evolutionary history of the parasite and its host. Parasites which
have colonized a new host species tend to be more virulent than
parasites which have coevolved with their hosts. Parasites which are
transmitted horizontally tend to be more virulent than those
transmitted vertically. It has been assumed that parasite-host
interactions inevitably evolve toward lower virulence. This is
contradicted by studies in which virulence is conserved or increases
over time. A model which encompasses the variability of parasite-host
interactions by synthesizing spatial (transmission) and temporal
(evolutionary) factors is examined. Lenski and May (1994) and Antia et
al. (1993) predict the modulation of virulence in parasite-host
systems by integrating evolutionary and transmissibility factors.

INTRODUCTION

Why do certain parasites exhibit high levels of virulence within
their host populations while others exhibit low virulence? The two
prime factors most frequently cited (Esch and Fernandez 1993, Toft et
al. 1991) are evolutionary history and mode of transmission.
Incongruently evolved parasite-host associations are characterized by
high virulence, while congruent evolution may result in reduced
virulence (Toft et al. 1991). Parasites transmitted vertically (from
parent to offspring) tend to be less virulent than parasites
transmitted horizontally (between unrelated individuals of the same or
different species). Studies in which virulence is shown to increase
during parasite-host interaction, as in Ebert\'s (1994) experiment with
Daphnia magna, necessitate a synthesis of traditionally discrete
factors to predict a coevolutionary outcome. Authors prone to
habitually use the word decrease before the word virulence are
encouraged to replace the former with modulate, which emphasizes the
need for an inclusive, predictive paradigm for parasite-host
interaction.

Evolutionary history and mode of transmission will first be
considered separately, then integrated using an equation discussed
by Antia et al. (1993) and a model proposed by Lenski and May (1994).
Transmission is a spatial factor, defined by host density and specific
qualities of host-parasite interaction, which gives direction to the
modulation of virulence. Evolution is a temporal factor which
determines the extent of the modulation. The selective pressures of
the transmission mode act on parasite populations over evolutionary
time, favoring an equilibrium level of virulence (Lenski and May
1994).

DOES COEVOLUTION DETERMINE VIRULENCE?

Incongruent evolution is the colonization of a new host species
by a parasite. It is widely reported that such colonizations, when
successful, feature high virulence due to the lack of both evolved
host defenses and parasitic self-regulation (Esch and Fernandez 1993,
Toft et al. 1991). Unsuccessful colonizations must frequently occur
when parasites encounter hosts with adequate defenses. In Africa,
indigenous ruminants experience low virulence from Trypanosoma brucei
infection, while introduced ruminants suffer fatal infections (Esch
and Fernandez 1993). There has been no time for the new host to
develop immunity, or for the parasite to self-regulate. Virulent
colonizations may occur regularly in epizootic-enzootic cycles. Sin
Nombre virus, a hemmorhagic fever virus, was epizootic in 1993 after
the population of its primary enzootic host, Peromyscus maniculatus,
had exploded, increasing the likelihood of transmission to humans
(Childs et al. 1995). Sin Nombre exhibited unusually high mortality in
human populations (Childs et al. 1995), which were being colonized by
the parasite.

It is assumed that coevolution of parasite and host will result
in decreased virulence (Esch and Fernandez 1993, Toft et al. 1991).
Sin Nombre virus was found to infect 30.4 % of the P. maniculatus
population, exhibiting little or no virulence in the mice (Childs et
al. 1995). Similar low levels of virulence have been found in the
enzootic rodent hosts of Yersinia pestis (Gage et al. 1995). In
Australia, decreased grades of virulence of myxoma virus have been
observed in rabbit populations since the virus was introduced in 1951
(Krebs C. J. 1994). Many of the most widespread parasites exhibit low
virulence, suggesting that success in parasite suprapopulation range
and abundance may be the result of reduction in virulence over time.
Hookworms are present in the small intestines of one-fifth of the
world\'s human population and rarely induce mortality directly
(Hotez 1995).

Evolution toward a higher level of virulence has been regarded
as an unexplainable anomaly. Parasites which do less harm presumably
have