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 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). TRANSMISSION AND THE DIRECTION OF MODULATION 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 available. 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 an …