Genotypebygenotype interactions

An individual's resistance depends on the species of parasite that infects it. Clones of Daphnia magna, for example, differ in resistance to two bacterial and three microsporidian parasites, and the pattern of resistance differs among the host's clones (Decaestecker et al., 2003). Resistance can also depend on the pathogen's genotype, so that some hosts are resistant against a subset of a parasite's genotypes while other hosts are resistance against other genotypes. An example of such genotype-by-genotype interaction is the gene-for-gene interaction, where resistance is controlled by pairs of matching genes (the resistance gene and the aviru-lence gene), which give resistance only if the host is homozygous for the resistance allele and the pathogen is homozygous for the avirulence allele. Gene-for-gene interactions are common in plants and their pathogens (Thompson and Burdon, 1992; Jones and Dangl, 2006), and have also been found in, for example, insect-parasitoid interactions (Dupas et al., 2003). Other types of genotype-by-genotype interaction underlie the resistance of snails to their schistosome parasites (Webster and Woolhouse, 1998), bumble bees to their trypanosome parasites (Schmid-Hempel et al., 1999), Daphnia to its bacterial parasite Pasteuria ramosa (Carius et al., 2001), and

Anopheles gambiae mosquitoes to the human malaria parasite Plasmodium falciparum (Lambrechts et al., 2005). In such a situation—whether resistance varies among parasite species or among parasite genotypes—'resistance' as the host's trait has no meaning; we can only discuss resistance of a given host against a given parasite and average resistance will change as the frequencies of the parasite species or genotypes change.

I will illustrate in more detail host-genotype-by-parasite-genotype interactions with the resistance of mosquitoes to malaria parasites (Lambrechts et al., 2005). The genetic variability of the major African vector A. gambiae was assayed by a comparison of the variability of resistance within and among full-sib families, a standard method of quantitative genetics (Falconer, 1989). Individuals of each family were challenged with one of several isolates of the human malaria parasite P. falcip-arum, which were obtained from naturally infected children in Kenya. Resistance was assayed as the likelihood that a mosquito harboured oocysts 8 days after infection and as the number of oocysts if there was at least one. For any given parasite, the mosquito families differed greatly in both measures of resistance (Figure 10.2); in any given mosquito family, the different isolates led to widely

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Figure 10.2 Graphical representation of the mosquito-family-by-parasite-isolate interactions underlying (a) the probability and (b) the intensity of infection. Each symbol represents the proportion of infected mosquitoes (in a) or the mean of the square root (Sqrt) of the number of oocysts (in b) for a given combination of family and isolate. The families are indicated on the x axes, and are separated into the three blocks of the study with vertical lines. Different symbols represent different isolates (open symbols show isolates containing two clones; closed symbols show isolates containing three clones), and the lines connect points representing the same isolate. Crossing lines give an indication of family-by-isolate interactions (from Lambrechts et al., 2005).

different levels of resistance, ranging in some families from 0% resistance against one isolate to 100% resistance against another. Averaged across all parasites, resistance was similar in all mosquito families, but the pattern of resistance against the isolates differed considerably among the families. In particular, no mosquito family was most resistant to all parasites, and no parasite isolate was most infectious to all mosquitoes. Thus, the level of mosquito resistance depends on the interaction between its own and the parasite's genotype; resistance is not a characteristic of the host that can be used as an indicator of general quality, but depends on the parasite the host is infected with. Any indicator of immune function is bound to give a misleading indication of the host's resistance, and indeed any measure of an individual's resistance (e.g. resistance against specific isolates, average resistance against all isolates) is bound to be a bad measure of its evolutionary success, for the overall resistance of an individual can only be defined for the parasites that happen to infect it and is thus determined by a combination of the host's genotype, the prevalence of each isolate, and chance.

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