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Factors of parasitic virulence

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Factors of parasitic virulence

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


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 ...

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Keywords: parasite virulence factors, factors of virulence and pathogenicity of microorganisms, parasitic factors that affect parasitism, factors of pathogenicity of bacteria, factors affecting pathogenesis

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