fundamentally from microparasites. Microparasites destroy tissue during
replication, and thus their virulence is directly related to replication.
In macroparasites, virulence is directly related to the density of worms
in the gut and, in high-density infections with high virulence, density-
dependent effects reduce egg production per worm (Fleming, 1988), so
there is no intrinsic benefit to increased virulence (Anderson and May,
1991). Indeed, virulence may be decoupled from transmission under
certain conditions. For example, inStrongylusspecies, nematodes that
infect orally before migrating through the body, virulence is not caused by
the adults but by the migrating larvae damaging tissue before they return
to the gut to reproduce. In these nematodes, there is no clear relation
between transmission and virulence (Medica and Sukhdeo, 2001).
However, in trichostrongyles, such asH. contortus, where adult worms
cause damage as they feed on tissue and reproduce, there is a positive
relationship between virulence and transmission rate (Medica and
Sukhdeo, 2001).Phylogenetic Constraints
Phylogeny undoubtedly constrains several aspects of nematode biology,
including habitat selection. However, while behavioural and life-history
characters are typically mapped on to existing phylogenies, they are
rarely included as character states in phylogenetic inferences. One of the
most perplexing aspects of nematode habitat selection is the superfluous
tissue migration before re-entering the gut. InStrongylus vulgaris, the
virulent caecal worm of horses, infection is oral, but the worms penetrate
the gut, migrate through the circulatory system and then return to the
intestines as adult worms (McCraw and Slocombe, 1976). At the heart of
this odd migration is the question of how parasitic nematodes evolved.
Nematode parasitism probably did not evolve until animals invaded
land, about 430 million years ago (Chabaud, 1954, 1955; Anderson, 1984).
Thus, there are almost no nematode parasites of marine groups, such as
molluscs, polychaetes and crustaceans, but a rich nematode fauna in
terrestrial groups, such as earthworms, insects and terrestrial molluscs
(Anderson, 2000). The entire group of monoxenic (one host) intestinal
nematodes are thought to have evolved from free-living, bacteria-feeding
soil nematodes, and the first mode of transmission was not by oral
ingestion but through skin penetration (Fülleborn, 1929; Adamson, 1986,
1989). In this scenario, nematode parasitism began with the accidental
penetration of the moist skin of an early amphibian host (Fig. 11.2). The
free-living nematodes probably already used the skin of an animal as a
mechanism to avoid dry periods in the environment and as transportation
between suitable habitats (Dougherty, 1951; Chabaud, 1982). After
penetrating the skin, the worms had to make the obligatory migration
to the gut because they were bacteria feeders, and the bacteria in the host
are found in the gut. Subsequently, large herbivores evolved and theyIntestinal Nematode Parasites of Vertebrates 235