Honey bees around the world have been dying at alarming rates, creating widespread concern and bafflement among both public and scientific communities. In the United States, symptoms of these impending declines are collectively referred to as Colony Collapse Disorder, or "CCD". CCD is primarily characterized by hive abandonment, where no or few honeybees are present in a hive even though a live queen remains. While many factors contribute to bee declines such as mites, viruses, bacteria, fungi, and pesticides, Dr. John Hafernik, a biology professor at San Francisco State University, discovered another contender by accident: the parasitoid fly Apocephalus borealis. With the help of colleagues and his graduate student Andrew Core (the lead author), the team worked to figure out this mysterious host-parasite relationship. Recently, their fascinating findings were published in pLoS one.
It turns out that female A. borealis flies will locate honeybee hosts and land on them, depositing their eggs or "ovipositing" them into the bee's abdomen. The fly larvae develop inside of the bee and approximately seven days later they emerge, killing the bee in the process. This is very reminiscent of the movie "Aliens" isn't it?
The parasitoid fly and it's honeybee host. A) An adult female Apocephalus borealis fly. B) A female A. borealis fly deposits eggs into the abdomen of a honeybee (note how small the fly is). C) Two A. borealis fly larvae exiting the host. Photo credit: Core et al. 2012.
The even more curious thing is that the parasitized bees exhibit very unusual behavior before fully succumbing to the parasites. They abandon their hives at night; healthy bees usually leave their hives during the day to forage. They wander about aimlessly in circles, appearing disoriented and unable to properly balance. Moreover, the bees become attracted to light at nighttime. Core and colleagues suggest that the parasites may manipulate the light sensitivity or circadian rhythm of their hosts in some way, but more work is needed to fully investigate these possibilities.
The troubling realization from all of this is that honeybees usually occur in high densities, and colonies are often found in close proximity to each other. These conditions could make it very easy for fly populations to boom and further decimate honeybee populations that are already in decline. Honeybees are crucial for the pollination of many plants and agriculturally important crops, and for the production of their highly prized honey. Research conducted by groups such as Core and colleagues is vital to the preservation of these important insects.
When I was an undergraduate at UC Santa Barbara I had the fortunate opportunity to take a parasitology course with Dr. Armand Kuris. During this intensive course we learned that parasites face unique challenges in life, and that our typical day is drastically different from that of a parasite. For example, we may wake up everyday and go to work or school, and come home for a nice dinner before going to sleep. For most of us, these activities are not exceptionally hostile experiences.
Consider the life of a parasite. A parasite must first encounter a host, which can be quite challenging if hosts are scarce or patchy, or not around at opportune times. Some infective stages only have a few hours to find a host before they perish in the environment. Next, the parasite must be compatible with it’s new host. Just because a parasite may find a potential home doesn't mean it will be able to live there. For example, have you ever been the unfortunate recipient of "swimmer's itch"? Perhaps you went for a dip in a lake or pond, only to be covered with small, intensely itchy bumps later on? That uncomfortable rash was caused by parasitic worms called trematodes (see below) that burrowed into your skin and tried to take up residence in your body. However, you were not a compatible host (these trematodes often use birds as their final hosts), and your immune system was able to quickly destroy the little invaders.
Another thing to keep in mind is that once a parasite successfully locates and enters an appropriate host, their new residence will soon try to kill them. Imagine living in a house that is alive and constantly assaulting you with the sole intention of ending your life. A parasite's life can be tough, and only a fraction of them may survive to reproduce.
How is one to thrive given so many obstacles? Parasites have evolved a variety of ways to locate hosts and once inside, many can combat or even evade the host immune system. They have conquered the host-time to celebrate! Well, not really. What if the parasite needs to leave it’s cozy home it worked so hard to obtain to complete its life cycle? This is the harsh reality faced by many parasites. Some must travel to mating locales that the host does not frequent, while others require transmission to additional hosts for their survival and reproduction. Still, others must find proper accommodations for their offspring inside an unwilling provider. This is when things get bizarre and where the science fiction writers come for ideas. This is why I am in graduate school.
Parasites that encounter these challenges will often hijack their hosts, manipulating their physiology, appearance, and/or behavior in ways that benefit the parasites. This phenomenon is termed “host manipulation”, and it has been identified in a wide variety of host-parasite relationships. Manipulations may be subtle (such as an increase in host activity levels) or spectacular (such as dramatic changes in host appearance and/or behavior). Although these manifestations are highly variable, the end result is often the same: the parasite prospers at the expense of the host. I have highlighted some cool examples below.
Zombie snails
Snails get infected with the Leucochloridium spp. parasite after inadvertently ingesting their eggs as they graze on contaminated vegetation. Once ingested, the trematode eggs release larvae called miracidia that develop into sporocysts which then form broodsacs that engorge the snail's eyestalks. These broodsacs contain hundreds of infective stages called cercariae that must get to a bird to complete the lifecycle. How will they get from a snail into a bird? The infested eyestalks begin to resemble caterpillars or grubs, and the broodsacs within pulsate when exposed to light! Birds searching for a meal may mistake these bags of worms for yummy insect larvae and go in for the kill.
Mind control by wasps
The Jewel Wasp (Ampulex compressa) mother has her work cut out for her. She must find a suitable host and somehow lure it back to her burrow where it will be held hostage, serving as a safe haven and living meal for her future offspring. What host would agree to this? Remarkably, this is not a problem for Jewel Wasps are they are powerful manipulators of the mind! When a female is ready to lay eggs, she locates an unsuspecting host for her young, usually a cockroach. She ambushes the roach, delivering a venomous sting into a specific region of it's brain. The neurotoxic venom does not paralyze the roach, but rather it makes the host submissive and seemingly undisturbed by the turn of events. The roach does not fight back, nor does it attempt to escape. Instead, it stands still while the wasp clips its antennae, drinking hemolymph ("insect circulatory fluid") from the open ends. Like leading a dog on a leash, the wasp grasps the host's antenna and leads it into her burrow. Once inside she will lay an egg on the zombified roach and the hatched larva will burrow into it's body, feasting on the internal organs. After five days or so, the larva will pupate and later exit the hollowed out carcass as an adult wasp.
Suicidal crickets
It is thought that "horsehair worms" (Phylum Nematomorpha) got their name from an old superstition that supposed the worms arose from horse hairs that fell into watering troughs. We now know that these worms do not arise from horse hairs, but are instead free-living adults that enter pools of water in search of mates for reproduction. As juveniles, the worms are obligate parasites that require an insect or crustacean for food and development (adults do not feed). However, a challenge arises once they mature and are ready to mate because their terrestrial hosts do not frequent aquatic habitats. How does one lead a cricket to water? Research suggests the worms chemically manipulate the central nervous system of their hosts, causing them to actively seek out watery areas. When the host eventually finds water it will jump in, stimulating the worm to exit the body, often killing the host in the process.
Additional reading sources:
1. D.G. Biron, L. Marche, F. Ponton, H.D. Loxdale, N. Galeotti, L. Renault, C.
Joly, and F. Thomas. 2005. Behavioural manipulation of a grasshopper
harboring a hairworm: a proteomics approach. Proc. R. Soc. B. 1577: 2117-2126.
2. C. Combes. 2001. Parasitism: the ecology and evolution of intimate interactions.
University of Chicago Press.
3. R. Gal and F. Libersat. 2010. On predatory wasps and zombie cockroaches:
investigations of "free will" and spontaneous behavior in insects. Commun.
Integ. Biol. 5: 458-461.
4. R. Gal and F. Libersat. 2010. A wasp manipulates neuronal activity in
sub-esophageal ganglion to decrease to decrease the drive for walking in its
cockroach prey. PLoS ONE 5 (4): e10019.
4. K.D. Lafferty and A.K. Morris. 1996. Altered behavior of parasitized killifish
increases susceptibility to predation by bird final hosts. Ecology 77: 1390-1397.
5. J. Moore. 2002. Parasites and the behavior of animals. Oxford University Press.
6. J.C. Shaw, W.J. Korzan, R.E. Carpenter, A.M. Kuris, K.D. Lafferty,
C.H. Summers, and O. Overli. 2009. Parasite manipulation of brain monoamines
in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis. Proc. R. Soc. B. 276: 1137-1146.
