Smart Mites

Parasitologists commonly observe species in which one sex is more heavily parasitized than the other. For example, territorial male impalas carry a much higher tick load than bachelor or female impalas (paper by Mooring and colleagues found here).  Territorial males spend less time grooming to remove ticks and instead spend their time watching for intruding males and wandering females.

Most of the explanations I’ve read for why one sex is more heavily burdened by parasites have focused on how host behavior, physiology and immune status influences their infection status. Few studies have examined if males or females have higher parasite loads because parasites are actively choosing one sex over another.

I was excited yesterday to come across this paper which examined whether or not parasitic mites are capable of preferentially infesting one sex. These researchers had previously observed that female bats from the genus Myotis are often infested with more mites than are males and so they decided to examine whether part of this pattern could be explained by the parasites “preferring” females.

Mites can not survive very long on their own and require a host for food and energy. It’s in the mite’s best interest to try to stay in areas of high bat density. This way they have plenty of other hosts when they reproduce and their offspring need to find a host of their own. It’s also a good idea to have other alternatives nearby in case the bat that the mite is currently living on falls ill and the mite needs to abandon ship.

If you’re like me, then when you imagine what bats you envision a cave wall with bats crammed in there nose to nose. The bats that roost in these large groups are females with their young. The males on the other hand, are loners. Instead of roosting with the group, they find a place to hunker down on their own. This means that, given a choice, mites should prefer to infest females who will surround themselves with other tasty bats over males encounter other bats far less frequently.

Researchers decided to test whether or not mites were capable of preferentially infecting females given a choice between both sexes. They placed a male and a female bat into an enclosed arena where their movements were limited and released a set number of mites into the enclosure. After keeping track of the mites’ choices, the researchers released the bats into an outdoor arena. Ten days later, the bats were recaptured and mite survival was quantified.

I know lots of people who don’t seem to know what’s good for them, but the mites seem to have it all figured out. The mites choose adult females significantly more often than they choose adult males AND their survival on female bats was much higher than on males.

The exact mechanism by which the mites differentiate between the sexes is unknown, but it’s likely that they’re using hormonal cues.

The more I learn about parasites the more amazed I am at how good they are at keeping themselves alive. This study showed that they’re capable of making good decisions when picking a host and I’ve discussed in a previous post how parasites are able to alter the behavior of hosts that they’ve successfully infected. I wouldn’t be surprised to find that the decisions made by parasites are driving differences in parasite loads between the sexes in lots of other species as well.

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

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.

The 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?

The 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

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

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!

 

The enemy of my enemy is my friend

An acanthocephalan parasite

Acanthocephalan parasites are infamous for their ability to dramatically alter the behavior of their hosts.  These parasites often have multi-stage life cycles, meaning that they die unless the host that they’re currently residing in gets eaten by the next host in the cycle. Acanthocephalans are remarkably efficient at manipulating their intermediate hosts into ending up on the dinner plate of the next host in the cycle. 

One well-known example of this manipulation involves the acanthocephalan parasite Polymorphus minutus and its crustacean intermediate host Gammarus roeseli.  The definitive host of P. minutus is a waterbird which scoops G. roeseli out of the water.  The usually defense by G. roeseli to avoid being consumed by the waterbird is to hunker down at the bottom of a streambed and hide in the rubble. The parasite is capable of counteracting this defensive mechanism, presumably by altering the concentration of serotonin in the crustacean’s nervous system. This manipulation causes the the host to swim to the water surface and clamp down on the surrounding vegetation.  In a closely related system (a different species of Gammarus and a different Polymorphus parasite), this behavior has been found to significantly increase consumption of infected gammarids by waterbirds.  In essence, the parasite causes its tiny host to swim up to where the predators are feasting and hang out until it becomes dinner. 

 

Gammarus roeseli

The interests of G. roeseli and the parasite P. minutus are clearly not aligned when it comes to waterbird predation. There is, however, one thing that they can agree on.  Neither of them want to end up in the stomach of other predators (fishes, crustaceans, etc.). Non-waterbird predators represent a dead end for both members of the party.  The old addage “the enemy of my enemy is my friend” goes a long way here, and recent studies suggest that the parasite enhances the host’s ability to stay out of harm’s way when their interests converge. 

Three-spined sticklebacks

Medoc et al. 2009 have shown that gammarids infected with P. minutus have a leg up on their uninfected counterparts when it comes to avoiding predation by three-spined sticklebacks.   Infected gammarids spent more time hiding in vegetation near the water surface and suffered much lower predation rates.  Additionally, another recent study found that infected gammarids are up to 35% faster when escaping a predatory crustacean.  

This phenomenon has received little attention in the literature.  The few studies that have looked at whether or not parasites “help” their hosts escape from mutually unfavorable predators have reported mixed results.  Some studies have found that infection increased the host’s susceptibility to all predators, whether or not they’re included in the parasite’s life cycle.  

The two studies decribed above showed that the gammarids could escape from predators if escape involved moving fast or hiding near the water surface. But, although the parasites have evolved an excellent host manipulation, it’s probably not perfect.

For example, in the above system where parasites make gammarids cling to water surface vegetation in order to be eaten by birds, it is likely that by doing so the gammarids become vulnerable to other predators. At that water level, there should be a number of other predators that can take advantage of the defenseless gammarids. How fine-tuned the parasite’s control of the gammarid can be is an interesting question deserving future study.

On another note, I’m heading to Santa Barbara tomorrow to meet Armand Kuris and Kevin Lafferty, two immensely awesome parasitologists who I hope to collaborate with for my dissertation work.  When I return on Thursday, I’ll surely have fun stories about the stuff I learned.  Wish me luck!

You are what you eat

One of the most interesting parasites is the protozoan Toxoplasma gondii. This sucker is everywhere and capable of some pretty amazing behavioral host manipulations.

 Nearly all warm-blooded organisms can be an intermediate host for this parasite. The parasite reproduces asexually in this host and forms cysts in its muscles and brain tissues. The parasite “wants” (in an evolutionary sense) its intermediate host to be consumed by its definitive host (wild and domestic cats) and has evolved elaborate mechanisms for altering its host’s behavior to make this happen. For example, infected mice become more active and more willing to spend time in open areas.

 Studies in rats have produced even more surprising results. Rats have an innate aversion to cat urine because it is usually a very good indicator that a predator is in the area. A study comparing rats infected with Toxoplasma gondii to uninfected controls discovered that not only do infected individuals lack the characteristic aversion response, but they actually seem to be drawn TO cat urine, a behavior which is certainly risky for a rodent.

 So parasites seem pretty capable of modifying the behaviors of rodents. But what about people?

 For many years, infection by Toxoplasma gondii in people wasn’t thought to be serious. Infected individuals would exhibit flu-like systems for a few days to a month or so, but after that would no longer feel “sick.” However, we now know that individuals remain infected because the parasite forms antibiotic resistant cysts that continue to reside in muscle and brain tissues.

 Recently, some labs have begun looking at whether or not Toxoplasma gondii has subtle behavioral effects that may have been overlooked in the past. Research is accumulating to suggest that this is indeed the case.

 Personality surveys have yielded mixed results, but the majority of surveys reveal that Toxoplasma gondii infected individuals exhibit significantly different behaviors than uninfected controls. For example, personality inventory results suggested that infected males are more vigilant, frugal, suspicious, jealous and less rule-following than male uninfected controls (any other women finding themselves wondering if particular ex-boyfriends were carrying heavy parasite loads??). Infected women, on the other hand, show a higher “superego strength,” meaning that they’re more moral, warm, persistent, rule-conscious and outgoing. These behavioral differences are more noticeable as time goes on.

 But that’s not all! Both infected men and women show higher apprehension, greater insecurity, and a decrease in novelty-seeking behaviors. Importantly, infected individuals appear to have slower reaction times than uninfected individuals. If you’re wondering whether or not the difference in reaction times is enough to matter, then consider the finding that infected individuals are 2.65 times more likely to be in a traffic accident than an uninfected individual.

 Finally, and perhaps most perplexing, is the finding that infected females are pregnant for a longer and are more likely to give birth to a son than a daughter.

 An important disclaimer should be made here. Because purposefully infecting people would be unethical, we can’t scientifically compare human behaviors before and after infection with Toxoplasma gondii. This means that it’s currently impossible to figure out whether this parasite induces the behavioral changes or whether individuals with a certain personality type are simply more likely to become infected.

 The jury is still out on the mechanism the parasite uses to induce these manipulations. Promising research suggests that manipulation of the dopaminergic system is to blame, but I’m not yet aware of anything conclusive.

 So how do people become infected in the first place? One common way to come in contact with the parasite is through the consumption of uncooked meats. Lots of warm-blooded animals contain infective Toxoplasma gondii cysts in their muscles, so countries in which people often enjoy undercooked meats have a higher occurrence of infection.

 Additionally, having cats around can increase infection risks. Toxoplasma gondii offspring are passed into the environment with a cat’s feces, where they become infective a few days later. Consuming the parasite and becoming infected can occur after changing a litter box or gardening (if cats have been defecating in the garden), for example.

 Infection rates in a population depend on diet and feline exposure, and infection rates have been reported to be as high as 80% in some areas. In the United Kingdom, for example, a report revealed that up to 38% of stored meat samples contained Toxoplasma gondii.

 These results have interesting implications! First of all, it’s almost scary to ponder whether or not some of the behavioral attributes that you consider to be quintessentially “you” are subtly modified by parasites. Second, how much of the differences between cultures can be explained by differences in infection rates? Might it be more dangerous to drive in countries where people eat a lot of uncooked meat, for example? Also, can information about how parasite behavioral manipulations tell us about how our brain works? Hopefully, the future holds more answers!

 Read more(!):

 Lots of work on this topic have been done by the Flegr lab and a review of their work on how Toxoplasma gondii effects human behavior can be found here.

 A review of the rodent literature by Joanne Webster can be found here.

 A paper on how Toxoplasma gondii may affect human culture by Kevin Lafferty can be found here.