Ecology, Epidemiology, and Evolution of Parasitism in Daphnia

  1. Introduction to the Ecology, Epidemiology, and Evolution of Parasitism in Daphnia
  2. Introduction to Daphnia Biology
  3. Some Parasites of Daphnia
  4. Parasitism in Natural Populations
  5. The Effects of Daphnia Parasites on Host Fitness
  6. Host Adaptations against the Costs of Parasitism
  7. Host Range of Daphnia Parasites
  8. Epidemiology
  9. Population Dynamics and Community Ecology
  10. Experiments with Daphnia and Parasites

6 Host Adaptations against the Costs of Parasitism

As parasites harm their hosts, the host may counteradapt, reducing the fitness costs of parasitism. Here I summarize the little we know about the ways Daphnia adapts to lower the costs of parasitism. One known example is that D. magna matures earlier in the presence of infections. I further discuss what is known about induced defense and the evolution of resistance in Daphnia. The chapter closes with a discussion of the limits of host resistance. Thus far, no evidence for a cost of defense has been found in Daphnia.

  1. Introduction
  2. Changes in Life History Traits
  3. The Evolution of Host Resistance
  4. Induced Defense
  5. Limits to the Evolution of Host Counter Adaptations
    1. Costs of Resistance
    2. Trade-offs between Defense Options
  6. Conclusions and Open Questions

6.1 Introduction

Parasites harm their hosts to foster their own needs. As studies thus far have shown, this damage varies across host clones, suggesting the presence of genetic variation among hosts for resistance or the expression of disease. This genetic variation for fitness-related traits may bring about different reproduction and survival rates among host genotypes, so that host clones that suffer less from parasitism increase their numerical representation in the host population. If at least part of the genetic variance for fitness is based on additive genetic variance, the host population may adapt to counteract parasites even across the sexual life cycle, i.e., even after the gene combinations in the clones are recombined into new genotypes.

Thus far, we have only a few clear examples of Daphnia hosts adapting to parasitism. There are two main problems with detecting host adaptations. First, if host adaptations lower parasite fitness (which is often but not necessarily always the case), parasites may rapidly evolve counteradaptations that reduce the effectiveness of the host adaptations and may make them invisible. A prediction of this theory is that host adaptations are more likely to be found in the presence of coevolving parasites if the adaptation benefits the host greatly but poses little or no disadvantage to the parasite. For example, the reduction of "unnecessary virulence", i.e., parasite-induced damage to the host that has no benefit for the parasite, could be an easily detected host adaptation (in novel, not yet coevolved, host–parasite associations, such unnecessary virulence is sometimes observed). Second, the adaptive value of host traits expressed in the presence of parasites may be difficult to judge because they stem from the interaction between two organisms and may or may not be beneficial to both (Moore 2002). For example, is the Daphnia’s parasite-induced change in diel vertical migration (Fels et al. 2004) beneficial for the host, the parasite, both, or none?

Host adaptations to parasites may be observed at several levels. The most impressive examples are those where a trait is expressed only in exposed or infected individuals and confers a benefit compared with individuals that do not express this trait. Examples of such phenotypic plasticity are early maturity and reproduction in exposed or infected females (Minchella and Loverde 1981). The same adaptation may, however, be constantly expressed within a host population (Jokela and Lively 1995). This may be beneficial if the host population suffers high rates of infection or if the constant expression of the adaptation has no associated costs in the absence of the parasite. Investigating constantly expressed host adaptations requires a comparison across host demes (populations) with variable degrees of parasitism and may require correction for common ancestry (Felsenstein 1985). If adaptations are thought to be host species or taxon specific, a comparative approach to the species or even to a higher taxonomic level may be required.

To verify that a host trait originates from host adaptation, one must carefully analyze the costs and benefits of this trait for both the host and the parasite. In some cases, this is rather straightforward, e.g., encapsulating and killing the parasite is obviously a host adaptation. It is, however, less simple in other cases, such as the enhanced growth of infected hosts, which some have suggested is adaptive for parasites (Baudoin 1975; Sousa 1983; Ebert et al. 2004), whereas others have argued that it is adaptive for the host (Minchella 1985; Ballabeni 1995). Below I discuss a few examples where there is good evidence that the traits observed are adaptive for the host.

6.2 Changes in Life History Traits

Although parasite-induced changes in host life history traits are frequently observed, most of them stem from the negative consequence of parasite exploitation (e.g., reduced fecundity and survival) and are not a host adaptation. The life history change that has received the most attention in various systems is the early reproduction of hosts that are exposed to or infected with parasites (Minchella and Loverde 1981; Jokela and Lively 1995). Early maturation has also been found in connection with two Daphnia parasites. In most D. magna clones, early maturation occurs when the host is infected early in life with the castrating bacterium Pasteuria ramosa (Figure 6.1

Figure 6.1
) (Ebert et al. 2004). This change in life history has been shown to benefit the host by increasing its lifetime reproductive success relative to infected hosts that do not show this response. Furthermore, early host maturation and reproduction harm the parasites by lowering the hosts’ transmission stage production because resources invested into host reproduction are not available for the parasite (Ebert et al. 2004). Likewise, Chadwick and Little (2005) observed that D. magna shift their life-history strategy toward early reproduction when infected with the microsporidium Glugoides intestinalis.

6.3 The Evolution of Host Resistance

Every Daphnia population tested for genetic variation in resistance has revealed high levels of clonal variation. Thus, Daphnia populations are probably under permanent selection for resistance. That they do not evolve efficient resistance suggests that the parasites have a high potential for evolving counter-resistance. However, clonal variation for resistance itself does not prove adaptive evolution. Experimental evolution has demonstrated that hosts do not evolve only in the presence of parasites but also that evolution proceeds very quickly.

Capaul and Ebert (2003) tested the extent to which parasite-mediated selection by different parasite species influenced competition among clones of the cyclic parthenogen D. magna. We monitored clone frequency changes in laboratory microcosm populations consisting of 21 D. magna clones. Parasite treatments (two microsporidians, G. intestinalis and Ordospora colligata) and a parasite-free control treatment were followed over a 9-month period. Significant differences in clonal success were found among the treatments as early as one month (about two to three Daphnia generations) after the start of the experiment (Figure 6.2

Figure 6.2
). The two parasite treatments differed not only from the control treatment but also from each other. The consistency of clone frequency changes across the replicates within treatments indicated adaptive evolution specific to the parasites used. The results suggest that parasites may influence microevolution in Daphnia populations even during short periods of asexual reproduction. A similar design was used by Haag and Ebert (2004), although in this study D. magna clones competed in mesocosms under outdoor conditions for one summer season. We also found rapid and significant changes in clonal composition across treatments.

These studies clearly demonstrate that microevolutionary change in Daphnia populations can be observed within short periods of time and that they are specific to the parasite treatment used. They did not, however, allow us to identify which traits were selected for, although it is reasonable that resistance to parasites played a role. In a follow-up experiment, we tested whether, under natural conditions, D. magna host populations showed higher levels of resistance after 2 years of evolution, including sexual recombination and diapause. The results showed that the hosts that evolved in the presence of the microsporidium Octosporea bayeri had a higher fitness than the controls in the presence of the parasites (M. Zbinden et al., manuscript in preparation). Fitness in this experiment was measured in a competition experiment that mimics the conditions under which the Daphnia evolved.

6.4 Induced Defense

A cost-effective way of protecting against invaders is to launch a defense mechanism only when challenged by a parasite or only under conditions where there is an increased likelihood of contracting disease. Little is known about the immune response of lower crustaceans, and because of their small size, it is difficult to study the physiology of the immune system. This will change when more genetic data become available (see, for example, Little et al. 2004).

A relatively easy way to investigate part of the immune system is through the prophenoloxidase (PO) system, which has received a lot of attention among ecologists interested in immunology, although it is not clear whether this system is more important than other aspects of the invertebrate immune system. The PO system has been used for testing hypotheses about induced defense; however, because it is believed to play a role in protecting invertebrate hosts from infections (Söderhall 1999). Mucklow and Ebert (2003) studied the system for Daphnia and showed that wounded D. magna, which presumably have a higher likelihood of contracting infections, have an up regulated PO activity. PO activity was also higher in well-fed animals than in poorly fed animals, suggesting that the expression of a high level of PO activity is costly. However, in a follow-up experiment, Mucklow et al. (2004) did not find that wounded D. magna, which presumably up regulated their PO activity, showed increased levels of resistance against the bacterium P. ramosa. Thus, a generalized induction of the PO system does not seem to reduce the risk of contracting disease.

Little et al. (2003) showed that induced defense may be highly specific. The hallmark of the vertebrate immune system is an acquired response against specific antigens. Memory cells resulting from a primary infection enhance the proliferation of antibodies during secondary infection. For invertebrates, an adaptive immune system with an immune memory has not yet been observed. Thus, invertebrates were believed to be naive at each new encounter with parasites. Little et al. (2003) found evidence for acquired immunity in D. magna infected with P. ramosa. Immunity was shown to be parasite strain specific to some degree. Host fitness was enhanced when the host was challenged by a P. ramosa strain that its mother had experienced relative to cases when mother and offspring were challenged with different strains. If this finding holds in general for Daphnia and other invertebrates, it would open a huge field of research for both the molecular mechanisms of acquired resistance and its evolutionary and ecological consequences.

6.5 Limits to the Evolution of Host Counter Adaptations

The evolution of defense against natural enemies may not come for free, i.e., there may be a trade-off between resistance (and/or tolerance) to parasites and other fitness components (Kraaijeveld and Godfray 1997). Such trade-offs may prevent the fixation of resistant genotypes and therefore could slow down or even prevent the evolution of resistance. This may explain why genetic polymorphism is maintained for resistance in the wild. Obviously, if the defense is more costly than the damage caused by the antagonists, it will probably not evolve. Even small costs of defense may slow down or hinder the evolution of defense because the costs may be paid permanently, whereas the enemies are encountered with only an uncertain likelihood. It may never pay off to invest in resistance against a rare parasite.

6.5.1 Costs of Resistance

Little et al. (2002) tested for the costs of resistance in a number of experiments with D. magna and P. ramosa but failed to detect any evidence for these costs. They tested whether resistant host clones have a reduced competitive ability or pay costs in the form of altered life history characteristics (e.g., delayed maturation, lower fecundity) in the absence of the parasites. They concluded that a cost of resistance is unlikely to explain the maintenance of genetic variation in the D. magnaP. ramosa system.

6.5.2 Trade-offs between Defense Options

Decaestecker et al. (2002) looked for a different form of cost of defense by studying habitat selection behavior, which is an important component of the Daphnia’s predator-avoidance strategy. The evolution of this behavior is often explained as a trade-off between avoiding antagonists and acquiring resources. Negatively phototactic clones suffer less from visually hunting predators because they reside deeper in the water column during the daytime. However, this behavior increases the risk of infections because they are exposed to pond sediments containing parasite transmission stages. Positively phototactic clones, which are at a higher risk of predation, are less exposed to parasite spores in the sediment and consequently suffer less from parasitic infection. The authors showed that the increased risk of infection also holds when the animals change their phototactic behavior upon exposure to chemical cues from fish. This study highlights a substantial cost of predator-induced changes in habitat selection behavior. Such trade-offs may explain genetic polymorphism for habitat selection behavior in natural Daphnia populations.

Speculating along the same lines, one may postulate that hosts have to trade off alleles for resistance against each other. If resistance requires certain alleles at a locus, the possession of one allele precludes the possession of another allele. Decaestecker et al. (2003) tested 19 D. magna clones for resistance against five parasite species to discover whether resistance against different species is traded off against each other. They were unable to find evidence for such trade-offs, although they found strong evidence for host–clone times parasite–species interactions. The same observation was reported by Carius et al. (2001) when they tested various combinations of D. magna clones with isolates of P. ramosa. Thus, the current evidence suggests that there is no trade-off for resistance against different isolates of parasite species.

6.6 Conclusions and Open Questions

The few examples given in this chapter show that Daphnia have evolved various ways of reducing the costs of parasitism. Some of these are likely to be phylogenetically old (evolution of immune response; PO system), whereas others seem to evolve very rapidly. The latter may play an important role in the host–parasite arms race (Ebert and Hamilton 1996; Ebert 1998a; Schmid-Hempel and Ebert 2003). Many fascinating questions about host adaptations remain unexplored, however:

  1. What is the underlying genetic system for the interactions between hosts and parasites?
  2. How many genes are involved in host resistance?
  3. Are there costs for resistance? What do these costs look like?
  4. Why is there no super-resistant host genotype?