Adaptive Value

Increased Lifetime Reproductive Success

Through the use of host manipulation the likelihood of being transmitted from the second intermediate host, the ant Formica fusca, to the third definitive host, such as cattle or sheep, is greatly increased (see Ontogeny for a more in depth explanation of this process). The host manipulation behavior therefore greatly increases the lifetime reproductive successes of the metacercariae infecting the ant, but with one unique case.

Altruistic Behavior Observed in the Brainworm

Each cercaria is capable of becoming a brainworm but only the first one to reach the subesophageal ganglion will do so. Experimentally, if every single cercaria is extracted from an infected ant and each implanted into a separate host ant they will all develop into brainworms. So, once one cercaria has committed to a costly host manipulation strategy all others will choose a cost-free nonmanipulative strategy. The cercaria that becomes the brainworm looses the ability to infect the third definitive host and reproduce, sacrificing itself for the benefit of the other cercariae. This is a perfect example of evolutionary altruism in nature. [6]

Altruism of this sort is defined as any behavior that benefits others (increases their chance of survival and thus their lifetime reproductive success) at the expense of the individual. In order to explain these cases of altruism the theory of inclusive fitness can be used. This theory states that in order to properly evaluate the fitness of an individual not only should the survival of the individual be examined but also how many of its genetic relatives (with each one weighted accordingly depending on their genetic distance from the individual) survive. Therefore, from an evolutionary standpoint, it would be worthwhile for a brainworm to sacrifice its own survival if such a behavior would result in the survival of a sufficient number of its genetic relatives. This strategy is called kin selection. This hypothesis states that whenever cases such as that of the brainworm are observed in nature, the explanation must be that the behavior being examined increases the survival, and with it the lifetime reproductive success, of a sufficient number of genetically related individuals. In this way even if the survival of the individual appears to be reduced the overall survival of its genes is being increased, thereby still resulting in a rise of its inclusive fitness. [6]

It is important to note that there is a definite possibility that the cercariae could actually be very unrelated, depending on what sporocyst and what adult the cercariae contained in one mucus ball come from. Therefore, depending on just how related the cercariae are, the strategy called group selection may be needed to explain this altruism of the brainworm. This hypothesis states that under the right set of circumstances (which can be precisely defined mathematically) it is in fact possible for altruistic behaviors to evolve between distantly related or unrelated individuals. [6]

Host Manipulation Diagram[5]

Figure 2. The probabilities of transmission and early death in the lancet liver fluke as a function of investment in the manipulation of the ant (i.e., manipulative effort, ME). If the brainworm did not invest in manipulation, the metacercariae would have a passive transmission rate (p) that is greater than zero but less than one. As the brainworm increases its investment in manipulation the transmission probability increases, but with diminishing returns for the brainworm (this depends on the genetic relatedness of the metacercariae). The cost of manipulation (loosing the ability to reproduce) and/or the probability of dying early because of the investment made in manipulation (the ant is more exposed to danger at the top of a blade of grass than in the mound) increase with the amount of investment. The total benefits of the brainworm equal m - p, which is the difference between the manipulated transmission rate (m) and the passive transmission rate (p). The optimal amount of investment in manipulation (ME*) for the brainworm is where the net gain (benefits minus costs) in transmission probability is maximized, that is, where the number of genetic relatives successfully reproducing outweighs the fact that the brainworm itself dies without reproducing and/or the chance that the ant dies before the metacercariae can be transmitted. [7]

One final remark about all of this is that host manipulation usually refers to a direct process in which a parasite incurs fitness costs in order to produce phenotypic changes in the host, but because it is possible to manipulate a host indirectly, a parasite could also alter phenotype without any fitness costs (besides those needed to survive in the host, such as host immune suppression) [10]. Also, in terms of effectiveness host manipulation should not be a measurement of the extent to which the host phenotype is altered, but instead by how much the altered phenotype increases the success of transmission of the manipulating parasite [7].

The Right Hatching Conditions

Lancet Liver Fluke EggThe lancet liver fluke is one of the few flukes that has a terrestrial life cycle, so it has evolved special adaptations to prevent desiccation during transmission, such as an embryonated egg (an egg containing a fully developed embryo) that won't hatch until it has reached the intestine of a snail [11]. It has been discovered that the complete absence of oxygen is a crucial requirement for successful hatching of the eggs. Experimentally, when placed in a chamber completely devoid of oxygen the rate of hatching reached a maximum when the amount of carbon dioxide in the chamber was between 0.1% and 4%. If even the smallest trace of oxygen were present the eggs would not hatch. Under natural hatching conditions bacteria in the intestine of the snail Cochlicopa lubrica ensure a consumption of oxygen and a production of carbon dioxide. In a laboratory setting eggs began to hatch about five minutes after being exposed to the optimum hatching conditions and continued to do so over the next 60-90 minutes [5]. The lifetime reproductive success of the lancet liver fluke thus also rests on the ability of the eggs to survive outside of any organism and to be successfully consumed by a snail.