Host manipulation by parasites: a spooky Halloween post

Happy Halloween! Turn on some spooky music, grab a handful of candy, and settle in for a spooky post about host manipulation by parasites! But do be careful eating; you never know when a parasite might be sneaking into your diet.

Cartoon of snails that look like Halloween candy because they have been manipulated by parasites.

What is adaptive manipulation?

If you’re a parasite enthusiast, you’ve probably heard about parasites that manipulate host behavior. But what, exactly, is host manipulation? We expect that infected hosts will often act “sick”; they might try to fight off their infections by raising their body temperature (fever) or eating medicinal plants, or they might be suffering from so much pathology from their parasites or immune responses that they lose their appetites, act lethargic, etc. But none of those sickness behaviors are adaptive manipulation. To be adaptive for the parasite, the changes to the host’s phenotype (coloration, morphology, and/or behavior) must produce a fitness benefit for the parasite, usually by increasing parasite transmission from one host to the next. Following this definition, the host’s phenotype is actually the parasite’s extended phenotype: the parasite’s genes control how the host looks or behaves.

To show that a host’s phenotype is an example of adaptive manipulation, we need to show that that the phenotype actually increases parasite transmission. This can be tricky! But here’s an example. Last week, we talked about the life cycle of Euhaplorchis californiensis, a trematode with a complex life cycle. The trematode infects killifish as the second intermediate host; specifically, it infects the hosts’ BRAINS. Infected killifish are more likely to do flashy swimming behaviors, like dashing up to the surface. This seems like an adaptive manipulation that would make infected fish more likely to get eaten by their definitive bird hosts; but how would you prove that? If you’re Kevin Lafferty, you’d put a bunch of killifish in two cages in the salt marsh, leaving one open to birds and one closed to birds. You can hear Kevin describe the experiment in this TED talk. At the end of the experiment, the cage that was open to birds had fewer infected fish than the cage closed to birds, because the infected fish with the flashy behaviors were more likely to be eaten than uninfected fish. The manipulated behavior increased transmission by increasing predation.

Most parasites that manipulate host behavior are not as well studied as Euhaplorchis californiensis. Therefore, we should be careful not to overstate adaptive benefits where they do not exist or have not been demonstrated, or to overdramatize demonstrated adaptive behaviors. For example, we often say that crickets infected with nematomorphs commit suicide by jumping into water, but not all crickets die or even lose the ability to reproduce after being infected. Furthermore, infected crickets aren’t so water-fixated that they hop in a straight line to the nearest waterbody; they’re just more likely to end up in water than uninfected crickets. It’s important to remember that many details tend to be glossed over when telling exciting and spooky stories, including those about parasites that manipulate host behavior.    

What kinds of manipulation exist?

We’ve mentioned a few examples, but how common is adaptive manipulation among parasites? We don’t know exactly how many parasites have evolved to manipulate their hosts, but we do know of a few hundred examples spread across many parasite groups (platyhelminths, acanthocephalans, nematodes, nematomorphs, arthropods, bacteria, fungi, protozoa, and even viruses). In fact, host manipulation mechanisms seem to have evolved independently many times within and between parasite groups. From this, we can conclude that adaptive manipulation is common, despite seeming so biologically bizarre.

But of course, there is spectacular variation among parasites in the ways that they manipulate their hosts. We can divide these methods into roughly five manipulation targets: predator avoidance, habitat choice, feeding or foraging, bodyguard behavior, and contact rates. I’ll explain each below.

Predator avoidance. Host manipulation seems especially common for parasites with complex life cycles that involve trophic transmission, where an intermediate host is consumed by a definitive host. In these systems, parasite transmission may be increased whenever the intermediate host becomes more conspicuous or less defended from the definitive host. Euhaplorchis californiensis is a good example of a parasite the manipulates how prey behave in the presence of predators.

Habitat choice. Sometimes parasites with complex life cycles have host species that do not share the same habitats or propagules (environmental stages) that require different habitats than the hosts, making it tricky for the parasite to make it from one host to the next. For example, larval nematomorphs infect terrestrial crickets and other arthropods, adults are free swimming in aquatic environments, and then larvae need to make it back to terrestrial environments to infect more arthropods. Nematomorphs manipulate cricket behavior to make them more likely to jump into water bodies—habitats that they would not usually choose. The story for how nematomorphs make it back to terrestrial environments might be even weirder, but the details are still being studied.

Host feeding behavior. Many parasites are consumed and/or transmitted during feeding, like those that are transmitted by blood-feeding insect vectors. If a vector only ever takes one blood meal, it cannot move parasites from one host to the next. To increase transmission opportunities, several parasites are known to affect vector feeding behavior, causing vectors to feed on more hosts and/or change their feeding behavior to increase the likelihood that a given feeding event will lead to transmission. A very different example might be trematodes that castrate their first intermediate snail hosts; snails reduce the time and energy that they spend reproducing when they are castrated, and instead spend that time eating, growing larger, and making more tissues available for the parasites to turn into more parasites. You can more read about parasitic castrators and gigantism in this blog post, including whether gigantism is truly adaptive for parasites.

Bodyguard behavior. Some parasites cause their hosts to co-opt normal behaviors or use abnormal behaviors to protect their parasites. For example, parasitoid wasp larvae cause orb weaving spiders to construct a protective web, and after eating the spider, the wasp larvae use the protective web as a safe hide out while they pupate. If you don’t go Google parasite bodyguards after reading this, you aren’t doing Halloween right.

Contact rates. Finally, although parasites with complex life cycles are usually the focus of adaptative manipulation research, parasites with direct life cycles and direct transmission might also benefit from manipulating host behavior. For example, if sexually transmitted parasites can cause their hosts to be more promiscuous, the parasites will be more likely to make it to a new host. It is unclear if there are few examples of this type of manipulation because it is understudied or because it is uncommon among directly transmitted parasites.

Now that you know what adaptive manipulation is and isn’t and what types of manipulation exist, you’re ready to go explore the many amazing examples that scientists have discovered or maybe to go discover a new example of your own! If you’re looking for good places to start, I recommend this TED talk by Ed Yong and this cartoon by The Oatmeal.

References:

Moore, J. Parasites and the Behavior of Animals. (Oxford University Press, 2002).

Poulin, R. Chapter 5 – Parasite Manipulation of Host Behavior: An Update and Frequently Asked Questions. in Advances in the Study of Behavior (eds. Brockmann, H. J. et al.) vol. 41 151–186 (Academic Press, 2010).

Simple versus Complex Life Cycles

When you first start learning about parasite ecology—and even decades later, when you’re an expert—parasite life cycles can be confusing! Parasite life stages have a plethora of fancy names, like L3 larva and miracidium, which can be difficult to remember. Furthermore, every parasite’s trajectory from immature to adult stages seems different than the last, and we don’t even know all the life cycle details for most parasite species. So, if you’re feeling confused by parasite life cycles, you’re in good company! You might never memorize all the complex life cycles that exist, but you can understand the general ecology and evolution of complex life cycles. We’ll cover the basics in this post.

Simple versus Complex Life Cycles:

Let’s start with simple life cycles, which are sometimes called direct life cycles or one-host life cycles. Monoxenic or homoxenous parasite species with simple life cycles only use a single host species in their life. The single host species is entered by infective stages of the parasite, and then the parasite grows and develops in the host before switching to reproducing within the host.

Direct life cycle parasites include parasites with fecal-oral transmission, like Ascaris lumbricoides, a roundworm that infects humans. Adult male or female roundworms live in the small intestine, where the female releases fertilized eggs into the environment through human feces. Eggs are ingested by people when they (usually accidentally) consume fecal matter. The parasite grows and develops in a series of larval stages in multiple tissues. The larvae eventually make their way to the respiratory system, where they are then coughed up and swallowed, which allows them to find their way to the small intestine to mature. This entire life cycle uses just a single host (humans), even as the parasite goes through many developmental stages inside and outside host.

This life cycle diagram for a simple life cycle parasite, Ascaris lumbricoides, depicts the parasite moving through several life stages from egg to larvae to adult, where the eggs exist in the external environment and the other life stages occur in the human host.

Now let’s move on to complex life cycles, which are sometimes called indirect life cycles or multi-host life cycles. Parasites with complex life cycles are indirectly transmitted from one host species to the next. These heteroxenic parasites need to use multiple host species in sequence to successfully develop and reproduce. Reproduction occurs in the final host in the life cycle, which is called the definitive host. The one or more hosts where parasite growth or development occur (but no reproduction occurs) are called intermediate hosts. Sometimes a parasite will not complete any life stages within a host, and instead only use the host for transportation; those transportation hosts are called paratenic hosts. The number of hosts needed to complete a life cycle is the life cycle length, and it must be at least two hosts long.

Ready for some examples? Schistosomiasis is caused by a parasite with a two-host life cycle, which uses humans as the definitive human host and snails as the intermediate host. Euhaplorchis californiensis is an example of a parasite with a three-host life cycle, which uses birds like herons as the definitive host, snails as the first intermediate host, and killifish as the second intermediate host. Life cycle lengths appear to have an upward limit, because most life cycles require four or fewer host species. Why do you think that is?

The life cycle of Euhaplorchis californiensis, a trematode that must sequentially infect three host species to complete its life cycle. This life cycle diagram came from The Ethogram Blog.

To get from one host to the next, parasites with complex life cycles can use a few different modes of horizontal transmission. Passive transmission occurs when the parasite just waits around for the next host, like when E. californiensis eggs in heron feces wait to be consumed by a salt marsh snail. Active transmission occurs when the parasite is free-living in the environment and moves around to seek out the next host, like when E. californiensis cercariae leave their snail host and swim around looking for a killifish to infect. And finally, complex life cycles often involve trophic transmission, where the parasite is consumed along with its intermediate host by the next host in the life cycle. Trophic transmission is used by all cestodes and acanthocephalans and many nematode and trematode species. Trophic transmission is probably so common in complex life cycles because predator–prey interactions are one of the most common ways that two (host) species might interact.  

Three ways to add hosts to a life cycle

You might have noticed that we need to make an important distinction between whether a parasite uses multiple host species in sequence, in parallel, or both. For example, E. californiensis does both: it must infect birds, snails, and killifish in that order to complete its life cycle, so it uses multiple host species in sequence. But it can also use multiple host species at a given life stage; in particular, E. californiensis can successfully infect and reproduce in more than one bird species. The number of host species that a parasite can successfully use for any given life stage is quantified as host specificity. Many complex life cycle parasites have high host specificity for some parts of their life cycle (e.g., they can only infect a single snail species as a first intermediate host) and low specificity for other parts of their life cycle (e.g., they can infect many bird species as definitive hosts).

This brings up an important question: how do host species get “added” to a parasite’s life cycle? We assume that parasite species start by infecting just one host species and then complex life cycles evolve from those simple life cycles. There are two ways that a host species is thought to be added in sequence, thereby increasing the life cycle length: upward incorporation and downward incorporation.

In upward incorporation, a new definitive host that is a predator of the original definitive host is added to the life cycle. Parasites that can infect the new predator without being digested are selected for because they have avoided a source of mortality. They also likely have higher adult body sizes, life spans, and fecundity inside the new definitive host, because the new definitive host species should be larger and longer-lived, on average, than the old definitive host species. After the new definitive host species is added to the life cycle, the parasite then represses reproduction in the old definitive host species, which is now used as an intermediate host. There is an upper limit to how long the life cycle can be made using upward incorporation, because there are only so many trophic levels in a given food web.

In downward incorporation, a new intermediate host that consumes free-living stages of the parasite and is consumed by the definitive host is added to the life cycle. (Yes, parasites are often eaten by predators!) This again reduces parasite mortality, because the parasites can now infect the new intermediate host instead of being digested. Since fewer parasite stages are lost to mortality and more make it to the definitive host via trophic transmission, overall transmission rates increase. Both downward incorporation and upward incorporation are thought to have led to the evolution of complex life cycles for some parasite species.  

This diagram from Parker et al. (2015) shows how a host is added to higher trophic level in upper incorporation and a lower trophic level in downward incorporation.

There is also lateral incorporation, where host species are added in parallel, making the parasite species less host specific (more of a generalist) for a given life stage. Parasites can benefit from infecting more host species in a given life stage whenever that makes them more likely to be able to find a host that they can successfully infect that can continue their life cycle. However, there are also some likely costs associated with being a generalist, instead of specializing on just one host resource.

Final thoughts

In summary, some parasite species have complex life cycles and some have simple life cycles. Some parasite species are highly host specific at every life stage and others are host generalists that seem to infect nearly everything. There’s a lot of variability in parasite life cycles, but in general, they can be described by their life cycle length and the transmission modes that parasites use to get from one host to the next. Beyond that, each life cycle diagram is just a bunch of fancy terminology.

If you’re new to parasite ecology and thinking about life cycles for the first time, I have a question to leave you with: how do you think scientists have figured out all these life cycles? If you found a new species of larval trematode in a fish, how would you figure out its life cycle?

References:

Parker, G.A., Ball, M.A. & Chubb, J.C. (2015). Evolution of complex life cycles in trophically transmitted helminths. I. Host incorporation and trophic ascent. J. Evol. Biol., 28, 267–291.

When Parasites Invade: A Need for Hosts

When the host of a parasite invades new territory, the parasite species might invade with it.  In a recent Journal of Parasitology paper, Novak and Goater (2013) explored how the lung fluke Haematoloechus longiplexus invaded Vancouver Island when it’s definitive host bullfrog (Lithobates catesbeianus) was introduced in the 1930’s and subsequently established in the wild.

H. longiplexus has a complex life cycle that requires three hosts.  Therefore, in order for H. longiplexus to establish in new territory, the two intermediate hosts must be present along with the invading bullfrog.

This life cycle of Haematoloechus medioplexus is very similar to that of Haematoloechus longiplexus. Photo Credit: Graphic Images of Parasites.

Physa snails are geographically widespread, and occurred in Vancouver Island before the bullfrogs invaded.  Furthermore, Novak and Goater (2013) found H. longiplexus metacercariae in six damselfly species in sites along the East coast of Vancouver Island.  Therefore, H. longiplexus went to Vancouver Island with its bullfrog hosts, and was lucky enough to find functional intermediate hosts already present.  Invasion success!

Interesting note:  No dragonflies had H. longiplexus metacercariae, so H. longiplexus is a damselfly specialist in Vancouver Island.  One explanation for this host specificity might be that when dragonfly larvae undergo metamorphosis, they lose their metacercariae, but metacercariae in damselfly larvae aren’t lost.  So, if a bullfrog snacks on an adult dragonfly, it won’t get infected, but if snacks on an adult damselfly, it might!

Its a snack, its a hat…
Photo Credit: Today.com

Can you think of any other reasons for host specificity in H. longiplexus?

Source:

Novak, C.W. and T.M. Goater.  2013. Introduced Bullfrogs and Their Parasites: Haematoloechus longiplexus (Trematoda) Exploits Diverse Damselfly Intermediate Hosts on Vancouver Island. Journal of Parasitology, 99(1): 59-63.