So far in this chapter we have focused on some of the studies of intraspecific populations that have helped to unravel patterns of dispersal and gene flow. We shall now look at some of the ways in which interspecific relationships can also influence movements of both plants and animals. One way in which this occurs is through plant-herbivore and predator-prey interactions, a classic example of this being plants that produce fruits that are palatable to frugivores. The rowan tree Sorbus torminalis is a temperate forest tree that is native to much of Europe. Seeds of this species will not germinate unless all of the fruit pulp has been removed, which often occurs when the fruit passes through an animal's intestine. Foxes, badgers, bears and several bird species, including thrushes and blackbirds, are all vectors that disperse rowan seeds. Long-distance dispersal is particularly likely to occur during the time (up to 12 h) that seeds remain in a bird's digestive tract (Oddou-Muratorio et al., 2001). An example of a predator-prey interaction that can influence dispersal is the abandonment of hoarded sawfly cocoons (Pristiphora erichsonii) by small mammals such as shrews and voles (Buckner, 1959). However, the direct dispersal of prey by predators is not a widespread phenomenon, and in animals the role of predation may be more important in determining whether or not individuals disperse (i.e. to avoid predators) or where they disperse to (i.e. to a predator-free site).
Dispersal can also be influenced strongly by parasite-host relationships. From the point of view of the parasite, dispersal is often at the mercy of its host (Figure 4.9). In one study, high levels of gene flow based on PCR-RFLP analysis of three polymorphic loci were found in the nematode Strongyloides ratti over a range of approximately 300 miles in the UK. This is a parasite of wild rats (Rattus norvegicus), and it is most likely the dispersal of juvenile male rats from their natal sites that prevents substantial population subdivision of either S. ratti or their parasites (Fisher and Viney, 1998).
A more detailed comparison of host and parasite dispersal emerged from a study of five parasitic nematodes from three host species in the USA: Ostertagia ostertagi and Haemonchus placei from cattle, H. contortus and Teladorsagia circumcincta from sheep, and Mazamastrongylus odocoilei in white-tailed deer (Blouin et al., 1995). Domestic sheep and cattle are moved regularly around the country, whereas white-tailed deer typically disperse over much shorter distances. Bearing in mind that these nematode parasites have no intermediate host and are unable to disperse in the free-living stage, it was not surprising that mitochondrial DNA revealed
Figure 4.9 Scanning electron micrograph of a parasitic water mite (Eylais sp.) that is being transported by its host, a water boatman (Sigara falleni). The movements of their hosts greatly facilitate the dispersal of these mites between waterbodies. Photograph provided by David Bilton and reproduced with permission
Figure 4.9 Scanning electron micrograph of a parasitic water mite (Eylais sp.) that is being transported by its host, a water boatman (Sigara falleni). The movements of their hosts greatly facilitate the dispersal of these mites between waterbodies. Photograph provided by David Bilton and reproduced with permission evidence for high gene flow in the sheep and cattle parasites. In contrast, there was evidence of subdivision and isolation by distance among populations of the white-tailed deer parasites, patterns that are compatible with restricted gene flow in hosts and therefore their parasites.
Dispersal patterns of hosts and their parasites are less concordant when the parasites have multiple hosts. Liver flukes (Fascioloides magna) live as adults in several herbivorous species, including white-tailed deer. They produce eggs in the liver of their host that then pass through the bile duct into the host's intestinal tract. Eggs are expelled in faeces, and those that successfully reach an appropriate water body will hatch into free-swimming larval flukes known as miracidia. The next stage in their development requires the flukes to pass into the body of a suitable snail species. Inside the snail, the miracidia develop into cercaria that, after several stages of growth, are released from the snail and encyst on aquatic or wet terrestrial vegetation. These cysts are then ingested by deer or other herbivores that eat the vegetation, and so the cycle begins again (Figure 4.10). An investigation into the population genetics of white-tailed deer and liver flukes revealed significant genetic differentiation among populations of both species, but the complex life cycle of F. magna meant that there was little agreement in the extent to which fluke and host populations from the same geographical regions were genetically differentiated (Mulvey et al., 1991).
While parasite dispersal often depends on the dispersal of the relevant hosts, it is also true that the dispersal of hosts may be influenced by the distribution of parasites. This is because a high parasite load at a particular site may cause hosts to move elsewhere. Male offspring of the common lizard Lacerta vivipara are more likely to disperse if their mothers harbour mites (Sorci and Clobert, 1995), and the kittiwake (Rissa tridactyla) is less likely to be faithful to a nesting site if there is a high level of tick infestation (Boulinier and Lemel, 1996). The great spotted cuckoo (Clamator glandarius) is a brood parasite, meaning that it lays its eggs in the nests of other bird species, which then rear the cuckoo's offspring, often at the expense of their own. In Europe, the main host of the great spotted cuckoo is the magpie (Pica pica). A study based on microsatellite markers revealed higher levels of gene flow among magpie populations living in sympatry with cuckoos compared with magpie populations living in allopatry (Martinez et al., 1999). This may reflect a greater tendency for magpies to disperse from populations that are parasitised by cuckoos.
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