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.

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

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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

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 an advantage throughout a long coevolutionary association with
their hosts. Ebert’s (1994) experiment with the planktonic crustacean
Daphnia magna and its horizontally transmitted parasite Pleistophora
intestinalis suggests that coevolution does not determine the
direction of the modulation of virulence. Virulence decreased with the
geographic distance between sites of origin where the host and
parasite were collected (Ebert 1994). Thus, the parasite was
significantly more virulent in hosts it coexisted with in the wild
than it was in novel hosts. Many viruses, such as Rabies (Lyssavirus
spp.), persist in natural populations while maintaining high levels of
virulence in all potential hosts (Krebs, J. W. 1995). Extinction is
not an inevitable outcome of increased virulence (Lenski and May
1994). Increased or conserved virulence during coevolution calls
into question long held assumptions about the effect of coevolution on
parasitic virulence (Gibbons 1994). Parasitic virulence frequently
changes over coevolutionary time, but the length of parasite-host
association does not account for the virulence of the parasite.
Transmission has been identified as the factor which determines the
level of parasitic virulence (Read and Harvey 1993).
Herre’s (1993) experiment with fig wasps (Pegoscapus spp.) and
nematodes (Parasitodiplogaster spp.) illustrates the effect of
transmission mode on parasitic virulence. When a single female wasp
inhabited a fig, all transmission of the parasite was vertical, from
the female to her offspring. The parasite’s fitness was intimately
tied to the fecundity of the host upon which it had arrived. When a
fig was inhabited by several foundress wasps, horizontal transmission
between wasp families was possible. In the figs inhabited by a single
foundress wasp, Herre found that less virulent species of the nematode
were successful, while in figs containing multiple foundress wasps,
more virulent species of the nematode were successful. Greater
opportunity to find alternate hosts resulted in less penalty for
lowering host fecundity. More virulent nematodes had an adaptive
advantage when host density was high and horizontal transmission was
possible. When host density was low, nematodes which had less effect
on host fecundity ensured that offspring (i.e. future hosts) would be

Low virulence is characteristic of many vertical transmission
cycles. Certain parasites avoid impairing their host’s fecundity by
becoming dormant within maternal tissue. Toxocara canis larvae reside
in muscles and other somatic tissues of bitches until the 42nd to 56th
day of a 70-day gestation, when they migrate through the placenta,
entering fetal lungs where they remain until birth (Cheney and Hibler
1990). A high proportion of puppies are born with roundworm infection,
which can also be transmitted from bitch to puppy by milk (Cheney and
Hibler 1990). If host density is low, a highly evolved vertical
transmission cycle (which exhibits low virulence in the parent)
ensures the survival of the parasite population.

High virulence is characteristic of horizontal transmission
cycles. In Herre’s (1993) experiment, more virulent parasites were
favored when host density was high and reduction of host fitness was
permissible. Certain parasites benefit from reduced host fitness,
particularly parasites borne by insect vectors (Esch and Fernandez
1993) and parasites whose intermediate host must be ingested by
another organism to complete the parasitic life cycle. By immobilizing
their host, heartworm (Dirofilaria immitis) and malaria (Plasmodium
spp.) increase the likelihood that mosquitoes will successfully ingest
microfilaria or gametocytes along with a blood meal. Heartworm
infestation causes pulmonary hypertension in dogs (Wise 1990),
resulting in lethargy and eventual collapse (Georgi and Georgi 1990).
Host immobility increases the opportunities for female mosquitoes to
find and feed upon hosts (Read and Harvey 1993). Infected dogs have
large numbers of D. immitis microfilaria in their circulatory systems,
again increasing the likelihood of ingestion by the insect. Many
infected dogs eventually die from heartworm, but in the process the
parasite has ensured transmission. Similar debilitating effects have
been observed in tapeworm-stickleback interaction; infected
sticklebacks must swim nearer the water’s surface due to an increased
rate of oxygen consumption caused by the parasite (Keymer and Read
1991). Parasitized sticklebacks are more likely to be seen and eaten
by birds, the next host in the life cycle.

Many horizontally transmitted parasites manipulate specific
aspects of host behavior to facilitate transmission between species.

Host fitness is severely impaired in such interactions. The digenean
D. spathaceum invades the eyes of sticklebacks, increasing the
likelihood of successful predation by birds (Milinski 1990). D.
dendriticum migrate to the brains of infected ants, causing them to
uncontrollably clamp their jaws onto blades of grass, ensuring
ingestion by sheep (Esch and Fernandez 1993, Combes 1991). Infection
of a mammalian brain by rabies (Lyssavirus spp.) alters the host’s
behavior, increasing the chance of conflict with other potential
hosts, while accumulation of rabies virus in the salivary glands
ensures that it is spread by bites (Krebs, J. W. et al. 1995).
Horizontally transmitted parasites which target nervous tissue
increase transmissibility by modifying the host into a suicidal
instrument of transmission.

Transmission factors determining parasitic virulence are the
spatial element in a spatial-temporal dynamic. Host density directly
determines the virulence of parasites which depend upon a single host
species (Herre 1993). Virulence may be increased when transmission
necessitates insect vectors or consumption of the primary host by
another species. Virulence varies inversely with the distance between
potential hosts; this distance is magnified when it is measured
between different species.

It has been proposed that there is a coevolutionary arms race
between parasite and host, as the former seeks to circumvent the
defensive adaptations of the latter (Esch and Fernandez 1993). In this
view, parasitic virulence is the result of a dynamic stalemate between
host and parasite. This exemplifies the red queen hypothesis, which
predicts continued stalemate until the eventual extinction of both
species. Benton (1990) notes that the red queen hypothesis ignores the
potential for compromise in such a system. Snails (Biomphalaria
glabrata) resistant to Schistosoma mansoni are at a selective
disadvantage due to the costs associated with resistance (Esch and
Fernandez 1993). A high level of virulence persists in the system
because the snail cannot afford to mount an adequate defense. The arms
race hypothesis assumes that the host population can successfully
counter increasing parasitic virulence with resistance over an
extended period of time. Although an arms race may be sustainable in
some fraction of parasite-host interactions, many hosts (such as B.
Glabrata) cannot participate indeterminately.

An alternative explanation for the reduced virulence of
congruently evolved hosts and parasites is the prudent parasite
hypothesis (Esch and Fernandez 1993), in which parasitic virulence
decreases in response to host mortality. Parasites which are too
virulent drive their hosts, and themselves, to extinction. Parasites
which are less virulent persist in the host population. The prudent
parasite hypothesis helps to account for the variation in
coevolutionary outcome by linking host population dynamics with
virulence, but it fails to describe the individual selective forces
which modulate virulence over time. The prudent parasite hypothesis
serves as the theoretical framework in which the factors determining
parasitic virulence can be synthesized. Antia et al. (1993) and Lenski
and May (1994) propose a tradeoff between transmissibility and induced
host mortality which predicts that parasites will evolve toward a
level of virulence which strikes an equilibrium in the parasite-host
system. Equilibrium models suggest that P. intestinalis, which evolved
a higher (yet appropriate) level of virulence in its host (Ebert
1994), is a prudent parasite. Antia et al. (1993) use an equation
developed by May and Anderson in 1983 to examine the tradeoffs in
parasite-host interaction: Ro = (BN) / (a + b + v). Ro is the net
reproductive rate of a parasite, B is the rate parameter for
transmission, N is host density, a is the rate of parasite induced
host mortality, b is the rate of parasite-independent host mortality
and v is the rate of recovery of infected hosts. Parasite populations
grow when transmission or host density increase, when host mortality
decreases or when hosts recover slowly. Studies have established a
positive correlation between transmissibility (B) and host mortality
(a) (Ebert 1994, Antia et al. 1993, Lenski and May 1994). Parasite
populations which exhibit high transmissibility (i.e. virulence)
within a host population are simultaneously lowering host density.
When host density is low, parasites which exhibit high virulence may
kill their hosts before contact with new hosts occurs. Thus,
transmissibility is a spatial factor which describes the likelihood of
contact between hosts and, ultimately, between a parasite and its

Lenski and May (1994) propose an evolutionary sequence in which
parasite populations adapt to the changes they cause in host density
(Fig. 1). A parasite suprapopulation is likely to include a range of
genotypes which are expressed in different potential levels of
virulence (Lenski and May 1994). When host density is high, more
virulent parasites are successful and host density is reduced. At a
lower density of hosts, less virulent strains of the parasite are at a
selective advantage as they increase host survival during infection
and allow more time for transmission to occur. Also, more virulent
strains of the parasite are prone to induce mortality in entire
subsets of the host population, driving themselves to extinction along
with their hosts. This pattern repeats over time, lowering virulence
with each adjustment to declining host population size. Extinction of
the host population is avoided when sufficient variation is present in
the parasite population (Lenski and May 1994).

The evolutionary sequence may be reversed to explain evolution
toward higher virulence when parasitic virulence is below the
equilibrium level. More virulent strains of the parasite outcompete
less virulent strains when host density is above equilibrium.

Conservation of virulence over time occurs when a stable equilibrium
is maintained. Conserved virulence may be high (Lenski and May 1994),
but it reflects stability within a system dictated by a unique set of
transmission factors. Many parasites must reach a certain population
size within the host to be successfully transmitted, while in certain
systems, sacrifice of one host facilitates transmission to the next
host (i.e. interspecies transmission). The inclusiveness of the
equilibrium model gives it great potential for accurate predictability
of a broad range of parasite-host interactions.

Traditional assumptions about the factors determining parasitic
strategy have been largely apocryphal, ignoring contradictory evidence
(Esch and Fernandez 1993). Equilibrium models synthesize the temporal
(i.e. evolutionary) factors and spatial (i.e. transmission) factors
characteristic of parasite-host systems. Time is required to modulate
virulence, while spatial factors such as host density and transmission
strategy determine the direction of the modulation.

The development of an inclusive, accurate model has significance
beyond theoretical biology, given the threat to human populations
posed by pathogens such as HIV (Gibbons 1994). Mass extinctions such
as the Cretaceous event may have resulted from parasite-host
interaction (Bakker 1986), and sexual reproduction (i.e. recombination
of genes during meiosis) may have evolved to increase resistance to
parasites (Holmes 1993). Parasitism constitutes an immense, if not
universal, influence on the evolution of life, with far-reaching
paleological and phylogenetic implications. A model which synthesizes
the key factors determining parasitic virulence and can predict the
entire range of evolutionary outcomes is crucial to our understanding
of the history and future of species interaction.

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