Disease transmission and personality

Thanks Jack and Jonathan for a push to get back in the saddle! Experiments have become manageable again (at least for a short period of time) and Zach and my parents have completed their summer visit. Time for SCIENCE!

Feral_CatOne topic that I find particularly interesting concerns how personality traits influence patterns of disease.  For example, people who are frequently stressed out are at a greater risk of becoming obese or acquiring heart disease. We often look at disease transmission at a population or community level, but I think individual level differences in behavior are a crucial and understudied area of research.

When diseases are transmitted from one individual to another, then social behaviors are an important factor in transmission dynamics. While it’s often difficult to study this phenomenon in humans, numerous social animals provide ideal study systems.

Natoli et al. 2005 is 0ne of the coolest studies that I’ve read on personality traits and disease. This research group examined 3 colonies of feral domestic cats in Europe and collected data on how male personality traits correlated with FIV (feline immunodeficiency virus) infection. According to the article, FIV infections in feral cats are usually lethal within approximately 5 years, at which point the cat’s immune system is too weak to fend off otherwise nonlethal infections.

FIV transmission occurs when one cat bites another, transmitting the virus from its saliva into the other cat’s bloodstream. Bites usually occur when two males are battling over territory or dominance rank or when a male bites a female during sex.

Feral_Cat_2In order to get a handle on the “personality” of the feral cats in each colony, the researchers logged hundreds of hours taking notes on the frequency with which each cat engaged in aggressive, submissive, affiliative, territorial, display or mating behaviors. They aggregated all of these measures and came up for a single score for each individual that indicated how “proactive” or “reactive” that individual was. Proactive cats more regularly marked their territory, were the most aggressive (often winning aggressive interactions) and often affiliated with other members of the colony. Reactive individuals rarely displayed aggressive behavior and were frequently submissive towards other members of the colony.

When the behavioral results were compared with information about which cats were infected with FIV, a clear patterns emerged. The males at the top of the hierarchy (i.e., the most proactive, dominant males) were the most likely to be infected with FIV. Their aggressive demeanor meant that they incurred bites more frequently than more submissive males, increasing the probability that aggressive males contracted the disease.

This finding brings up a logical question. If all of these aggressive cats are contracting terminal diseases, why are aggressive cats still around? Well, the first answer to that question lies in that fact the cats don’t succumb to the illness quickly. The disease has a long asymptomatic period during which the cats continue to strut around as if nothing is wrong.

Importantly, aggressive behavior also maintains access to the ladies. Paternity tests revealed that the proactive cats were fathering a lot more of the kittens than the reactive males. Because aggressive dads produce more offspring than submissive dads, we might not expect aggressive behavior to be diminishing anytime soon.

This was a particularly nice study because it examined multiple populations (lending support to the generality of the results), measured lots of behaviors and included a direct measure of evolutionary fitness. It’s rare to find so comprehensive a study.

When dealing with socially transmitted diseases, personality plays a large role in the number of times an individual may be exposed to an infectious agent. In the study described above, aggressive behavior was the key to transmission. In other systems the important relevant measures may be frequency of sexual behavior, energy put into hygiene, number of individuals with which one associates, etc. Personality plays a large role in determining the diseases to which one is most susceptible.

Advertisements

To kill a killifish

For my dissertation I’m planning on studying California killifish and Euhaplorchis californiensis, my favorite host/parasite system.  The Kuris Lab has done some really excellent work on this system,  providing a great foundation for future studies. 

Euhaplorchis californiensis is a trematode parasite with a complex life cycle.  Its life starts in the digestive tract of waterbirds, where it remains for only a short time before being defecated. Shitty way to start off, huh?   

Cerithidea californica

Cerithidea californica

The horn snails, the parasite’s next host, aren’t especially perceptive and consume E. californiensis while grazing along the bed of the estuary. Once infected, the parasites castrate their snail host and turn the snail into a parasite-making factory.  After a few parasite generations, a significant portion of the snail’s mass will be E. californiensis offspring. When the parasite has completed development, it burrows out of the snail and swims into the water column.

C.californica_parasitizedThe picture on the left is of a deshelled, parasitized horn snail.  If you click on the picture to enlarge it, you’ll notice that much of its back half is white and it almost looks like it’s filled with small grains of white rice.  It’s actually filled with a bunch of trematode parasites (though in this case it isn’t E. californiensis).  

The parasite’s next target is the California killifish (Fundulus parvipinnis).  When a killifish is unfortunate enough to run into the parasite, the parasite will burrow inside and make its way up to the fish’s brain.  Research on closely related species suggests that the parasites find a nerve and follow it up to the brain.  

This is where it gets cool. 

Jenny Shaw and her collaborators looked at how neurotransmitters in killifish brains change as parasites accumulate (the paper can be found here).  They found significant changes in the concentrations of two neurotransmitters, dopamine and serotonin, and found that these changes were more pronounced as parasite density increased.  

One striking finding was that the parasites were suppressing a common stress response.  When vertebrates are stressed, a part of the brain known as the raphe nuclei increases its rate of serotonin metabolism, which essentially means serotonin levels decrease in this part of the brain.  In infected killifish, serotonin levels decreased much less, indicating that the parasites are affecting their host’s responses to stressful situations. As encounters with a predator are clearly stressful, this may be an important mechanism used by the parasites to get the killifish eaten by its next host.  

This poses an interesting possibility – are the parasites altering killifish behavior to make them more likely to be eaten by a particular animal?

Male killifishThe answer is yes, infected killifish do exhibit strange behaviors that make them significantly more likely to be comsumed by waterbirds, the definite host (that is, the host in which the parasite reaches maturity) of E. californiensis.  Lafferty and Morris 1996 observed that infected killifish frequently engaged in behaviors that made them quite conspicuous, including quick trips up to the water surface (which could make the killifish into a quick meal for an awaiting waterbird).  They then set up outdoor enclosures containing killifish that they knew to be infected and those that were uninfected.  Waterbirds were capable of accessing the fish in the enclosure and twenty days after the enclosures were set up the researchers returned to see who was left. 

The results were staggering.  Infected killifish were 30 times more likely to have been consumed by waterbirds than the uninfected fish!  This is immensely strong evidence that the parasites are adaptively manipulating their hosts.  

Much remains to be learned about this system, but parasites like E. californiensis which are capable of behavioral manipulation may tell us important things about how our brain works and perhaps even provide insight into treatments for certain behavioral disorders.  Many behavioral disorders including depression and bipolar disorder are thought to be associated with inappropriate concentrations of neurotransmitters such as dopamine and serotonin in the brain. Understanding how parasites manipulate the concentrations of these chemicals may teach us how we can alter them as well.   

At the moment, we don’t know how parasites are changing neurotransmitter concentrations in the brain.  They could either be secreting the chemicals themselves or they could be manipulating the brain into doing it for them. If they’re manipulating the brain, then the method that they use to do this could provide us with new treatment ideas.

Here comes the fun, wild speculation part. If the technology for nanobots ever gets off the ground then we could use parasites as a model for how to make small-scale changes to neurotransmitters as a way to control behavioral disorders. Alternatively, I wonder if we could create genetically modified parasites capable of altering the concentration of a particular neurotransmitter in specific parts of the brain.  Parasites already know how to get to the brain on their own and we know that controling the number of parasites controls the intensity of the changes in neurotransmitters.  So why not give it a shot (in animal models first, of course)?

California killifish

California killifish

Parasites: a weighty topic

Hey there, blogosphere!  I’m finally back in town and have caught up on the work that I missed while visiting the Kuris Lab at the University of California-Santa Barbara. This group of parasitologists addresses numerous interesting parasite-related questions, including those related to the importance of parasites in food web dynamics and the potential applications of trematodes as bioindicators.  

 

Carpinteria Salt Marsh in Santa Barbara

Carpinteria Salt Marsh in Santa Barbara

Recently, this group intensely studied 3 estuaries and calculated the biomass of the species found at each site.  The prevailing opinion at the time of this study was that parasites are probably not found in high enough abundances to play an important role in ecosystem energetics.  You can imagine how surprised everyone was then when the Kuris Lab showed that parasite biomass was often greater than the biomass of much larger groups of animals.  For example, if you stuck all of the trematode parasites found in an estuary on one scale and all of the estuarine birds on another, you’d find that the parasites weight 3 to 9 times (depending on the estuary) MORE than the birds!  These findings were published in Nature.

 

I think that studies like this are of immense importance because they change the way that we think about parasites.  Parasites capture our imagination by doing things to their hosts that are more gruesome and amazing than just about anything science fictions writers have come up with thus far.  Because of this, I think we tend to think of them as interesting anomalies and forget that parasites make up more than half of the species found on the planet.  Future work will surely continue to enforce that parasites are important in numerous ecological processes and in human culture.  

Next post: The Kuris Lab’s work on brain altering parasites in killifish!