Study ties kin selection to host-manipulating behavior in parasites

In essence, when it comes to successful transmission, some parasites get by with a little help from their kin.

Specifically in the case of lancet liver flukes (Dicrocoelium dendriticum), a single larva travels to and takes over its ant host's brain, compelling the ant to cling to vegetation until it is eaten by the fluke's next host, a grazing mammal such as cattle and deer. In a textbook example of altruistic behavior, the brain fluke sacrifices itself to ensure the survival of its relatives, who co-infect the same ant's abdomen. Ant exposure via vegetation ensures transmission of the abdomen flukes, who live on by infecting the mammal's bile ducts, where they sexually reproduce and send the next generation of parasite progeny out into the world ensconced in host feces.

For more than 40 years, scientists have hypothesized kin selection -- the evolution of traits that favor survival of relatives -- to explain the brain fluke's noble self-sacrifice.

"It was presumed that genetically identical individuals, which we call clonemates, can end up in the same ant because in the snail first host, there is an asexual reproductive stage of the parasite," Criscione said. "Many larval parasites that are clonemates are released from the snail in a slime ball that ants like to eat. However, no one has tested the clonal relationships of the parasites co-infecting ants, especially between the brain fluke and abdomen flukes."

Criscione and colleagues Dr. John Gilleard (University of Calgary) and Dr. Cam Goater and Dr. Brad van Paridon (University of Lethbridge) did just that, and they now have the data to prove it.

In their study that measured genetic relatedness between brain and abdomen flukes within ants, the team was able to show not only that clonemates simultaneously occur in the same ant much more often than expected by chance, but also that the brain fluke commonly has clonemates within the same ant. Their research, currently published online and set to be included in next week's issue of the Proceedings of the National Academy of Sciences, provides rare genetic evidence to support a role for kin selection in the evolution of an altruistic, host-manipulating behavior that facilitates parasite transmission and as an evolutionary explanation for similar behaviors that improve the odds of survival and reproduction among genetically related family members.

"The lancet fluke is an extreme example of kin selection in that the asexual reproductive stage of the parasite in its snail host has enabled the highest degree of genetic relatedness; i.e., clonality," Criscione said. "While our data confirm the original hypothesis in that we find lots of clonemates and that these clonemates co-infect the same ant, our study also reflects the important need in science to collect hard data where possible to test our hypotheses regardless of how intuitive something may seem, especially in iconic systems such as the lancet fluke."

To explain kin selection, Criscione defers to one of the founding fathers of population genetics, J.B.S. Haldane -- specifically, a quote recalled by his graduate student and prominent evolutionary biologist John Maynard Smith, ascribed as follows: "I would lay down my life for eight cousins or two brothers." Essentially, a trait that reduces one's own survival and/or reproduction -- an altruistic trait -- can increase in frequency in the population because the trait benefits the survival and/or reproduction and therefore the individual fitness of one's relatives.

"Full siblings and first cousins share on average 50% and 12.5%, respectively, of their genetic information," Criscione said. "By 'helping' two of one's full siblings or eight of one's cousins, the individual is in effect ensuring the survival and/or reproduction of itself, from a genetic information perspective.

"Theory indicates that a truly self-sacrificing behavior -- altruism -- cannot evolve by natural selection because the actor dies and cannot pass on the genetic variant(s) underlying the behavior. However, if the recipients of the actor's altruistic behavior are related to the actor, then the trait can evolve, or increase in frequency, because the actor shares its genes with its relatives. This is the premise of kin selection, or the evolution of traits that benefit one's relatives. We found the brain fluke has clonemates in the abdomen, so even though the brain fluke does not transmit to the next host, its clonemates, which are akin to twins because they share 100% of their genetic information, do."

Interestingly, Criscione notes that when the ant first eats the snail slime ball and ingests myriad parasite larvae, many migrate to the ant's head. But when one reaches the ant's brain, the rest change direction and migrate to the abdomen, where they form a protective cyst around themselves.

So what makes that one brain fluke turn hero, much less the others turn back and head for the comparative safety of the ant's abdomen?

"We do not know," Criscione said. "A hypothesis is that the genetic basis of this 'hero' trait is found in all individuals, but we need to know the gene or genes that control the trait to answer this. Thus, it remains an outstanding question. As for the change in direction, a hypothesis there is that either the brain fluke directly releases a chemical or the brain fluke indirectly causes the ant to release a chemical that informs the other larvae to go to the abdomen."

From a broader perspective, Criscione says the melding of kin and multilevel selection has rekindled interest in how genetic relatedness among individuals influences selection on traits, ranging from social behavior to how plants grow roots.

"Our study adds a unique trait to the list where the kin-selected trait is one that facilitates parasite transmission," Criscione said. "It is also interesting for trematodes, which are a diverse group of parasitic flatworms with more than 30,000 estimated species -- some of which are of major economic and health importance. All trematode species have asexual reproduction in their first host, which is usually a mollusk such as snails. Thus, clonality, the highest form of genetic relatedness, makes kin selection a possibility in the evolution of other trematode traits, including competition among clones and caste formation, or possibly even their hosts with regard to virulence."

Criscione says there is much to be learned about the transmission biology of clonemates within the lancet liver fluke system, from how many make it to the final mammal host to how dispersed they are among individual final hosts.

"If clonemates end up in the same host and mate, this is equal to self-mating," Criscione said. "Self-mating is an extreme form of inbreeding, which is one of the evolutionary mechanisms that shapes how genetic information is partitioned among individuals in a population. Moreover, it will be of interest to ask if any particular clone dominates, or do we see a mix of different clones surviving the transmission process to the final host?"

Because altered host phenotypes -- behavioral and morphological -- by parasites occur in other parasite groups beyond trematodes, Criscione says it will be important to merge the ecology, population genetics and phylogenetics of the parasites with these parasite manipulation traits to fully understand their origins, adaptive significance and ecological context.

"Parasites are extremely diverse in terms of their ecologies and the number of different species that have evolved a parasitic life cycle," Criscione added. "Therefore, it will be exciting to discover the possible ways by which altered host phenotypes have come about across the different parasites."