Download Supporting Information Parasite-mediated selection and its effects

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Supporting Information
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Parasite-mediated selection and its effects on host diversity
Parasites can exert a number of different types of selection on host populations, leading
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to either increased or decreased host diversity. Specifically, parasites can increase host diversity
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via negative frequency dependent selection or disruptive selection; parasites can decrease host
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diversity via stabilizing selection, directional selection for increased resistance, or directional
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selection for increased susceptibility (see main body of article; Figure 1).
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When determining the type of selection experienced by a population, two pieces of
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information are useful. First, it is important to know whether there are host-parasite genotype
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interactions, since these are a prerequisite for negative frequency dependent selection. Studies
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looking for such interactions usually expose a range of host genotypes to a range of parasite
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genotypes, and test for significant host genotype x parasite genotype interactions (e.g., Carius,
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Little & Ebert 2001, Salvaudon, Heraudet & Shykoff 2007). Second, changes in the distribution
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of susceptibilities (that is, how easy it is to infect a genotype) in the host population should be
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measured. In many cases, these changes are measured as changes in mean and/or variance (e.g.,
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Brockhurst et al. 2003, Duncan, Mitchell & Little 2006), but the overall distributions of
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susceptibilities can be compared as well (e.g., Duffy et al. 2008).
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When measuring changes in the distribution of susceptibilities, a key question is what
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parasite genotypes to use when assaying susceptibilities. Frequently, a mixture of different
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parasite genotypes are used (e.g., Brunet & Mundt 2000, Herzog, Müller & Vorburger 2007). In
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general, the parasite genotypes used should be as representative as possible of those causing the
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selection.
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It is interesting to note that many studies, and particularly those looking for negative
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frequency dependent selection, use a third approach as well – mathematical models
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parameterized for the specific study system (e.g., Decaestecker et al. 2007, Dybdahl & Lively
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1998). This suggests that combining empirical and theoretical approaches may be a particularly
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powerful way to study the effects of parasites on host populations.
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It is also possible to test for parasite-driven evolution using the Lande-Arnold selection
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gradient method (Lande & Arnold 1983), though this approach is less common. One study used
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this approach to look for selection on two species of cactus, Echinopsis chilensis and Eulychnia
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acida driven by a parasitic mistletoe, Tristerix aphyllus (Medel 2000). In this case, there was
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only weak or no selection on a trait hypothesized to be important to resistance (spine length).
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This method is quite powerful for detecting directional, stabilizing and disruptive selection;
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however, it requires the ability to measure both the phenotype and fitness of individuals in the
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field (Lande & Arnold 1983), making it difficult to apply to many organisms.
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In Figure 1, we show expectations for the patterns of susceptibility as measured in natural
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populations. We present the case for a disease with epidemic dynamics because there is a clear
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period during which selection occurs. Much of the theory, however, considers parasites that are
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endemic. We expect the qualitative changes in the population to be the same for endemic vs.
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epidemic diseases, though this is an area worthy of further exploration.
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In most cases in Figure 1, we assume that the population has an approximately normal
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distribution of susceptibilities prior to an epidemic, though this will not necessarily be the case.
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However, for negative frequency dependent selection, a normal “pre-epidemic” distribution is
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not expected. Rather, the most common genotypes should be the most susceptible, since the
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parasites best at infecting those genotypes should be the most common (Bell 1982, Hamilton
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1980, Jaenike 1978). Therefore, in the case of negative frequency dependent selection, the pre-
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epidemic distribution should be skewed so that the highly susceptible genotypes are also the
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most common.
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Uses of the term “frequency dependent”
While the theoretical literature has clearly shown that parasites can exert different types
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of selection on their host populations, many empiricists remain unaware of several of the
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possibilities (most notably the possibility of parasite-mediated disruptive selection). We suspect
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that the dominant reason for this is simply that some of the possibilities (such as disruptive
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selection and selection for increased susceptibility) are initially counterintuitive, at least if trade-
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offs are not explicitly considered. However, another factor that is likely contributing to the
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confusion is the different uses of the term “frequency dependent” in the host-parasite literature.
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In this regard, the host-parasite literature mirrors the broader literature, where frequency
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dependent is used to refer to very different mechanisms (Heino, Metz & Kaitala 1998). This
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potential confusion is important in the context of the present review, since the nature of
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transmission can affect evolutionary outcomes (see below).
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In general, the term “frequency dependent” is used more broadly in the theoretical
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literature than in the empirical literature (where it is generally used in reference to negative
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frequency dependent selection). In its broadest sense, frequency dependent selection refers to
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the idea that the fitness of a genotype depends on the other genotypes present in the population
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(Futuyma 1998), which is generally true in host-parasite interactions. This can be best
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understood in light of disease thresholds, which arise because a certain fraction of individuals
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must be susceptible to a disease in order for the disease to invade that population (that is, in order
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to be above the disease threshold; Anderson & May 1991, Keeling & Rohani 2008). For
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example, if a population is dominated by highly resistant phenotypes (and, therefore, is below
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the disease threshold), the fitness of a highly susceptible phenotype is likely to be higher than in
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a population dominated by susceptible phenotypes (where the parasite is able to persist and
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attack our focal phenotype). In this case, then, the fitness of a phenotype depends on the other
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phenotypes in the population, not because those other phenotypes determine the parasite strain
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that dominates the population (as with negative frequency dependent selection), but because
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those phenotypes help determine whether the parasite is present in the population at all. It is in
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this sense that the term "frequency dependence" is generally used in the theoretical host-parasite
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literature, including in the adaptive dynamics literature (Waxman & Gavrilets 2005).
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As discussed in the main body of this article, negative frequency dependent selection can
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arise when there are host-parasite genotype interactions – that is, when the susceptibility of a
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particular host genotype depends on the parasite genotype to which it is exposed. In this case,
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parasites "track" the common host genotypes, which reduces the fitness of those common
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genotypes and favors rare genotypes (Woolhouse et al. 2002). As a result, the fitness of a
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genotype decreases as its frequency increases, because the parasites that are best at infecting that
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host genotype become common. When empiricists discuss “frequency dependent selection”, it
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generally is in reference this more specific case of negative frequency dependent selection.
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Finally, "frequency dependent” is also used in the host-parasite literature when describing
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disease transmission (Begon et al. 2002, de Jong, Diekmann & Heesterbeek 1995, Grassly &
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Fraser 2008). Generally, two transmission terms are considered: density dependent transmission
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and frequency dependent transmission (Keeling & Rohani 2008). With density dependent
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transmission, transmission is assumed to scale with the density of hosts; that is, the rate of
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increase of infected hosts is described by βSI, where β is transmission rate, S is the density of
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susceptible (that is, uninfected) hosts, and I is the density of infected hosts. In contrast, with
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frequency dependent transmission, the rate of increase of infected hosts is assumed to scale with
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the frequency of infected hosts: BSI/N, where N is the density of the host population. Frequency
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dependent transmission is considered particularly common for sexually-transmitted diseases
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(Anderson & May 1991, May & Anderson 1979), but has also been found in diseases that are not
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sexually transmitted (e.g., measles in humans: Bjørnstad, Finkenstädt & Grenfell 2002; cowpox
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in voles and mice: Begon et al. 1999). Whether disease transmission is density dependent or
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frequency dependent can affect the evolution of host resistance (Antonovics & Thrall 1994).
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Specifically, Antonovics and Thrall found that directional selection for increased resistance was
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more likely with density dependent transmission, whereas disruptive selection (leading to
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coexistence of resistance and susceptible genotypes) was more likely with frequency dependent
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transmission.
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