Sex Matters

Because of the differences between male and female physiology, males and females can have different reactions to the same parasite. These variable responses can have important consequences for parasite-host interactions and the overall transmission of the parasite. Take, for example, a relatively recent study of great tits (Parus major, a bird).

Dunn et al. (2011) explored the effect of malarial infection on the behavior of male and female great tits. While the differences between males and females are obvious in many species, sex-specific differences in behavior due to infection are not often investigated. Anyway, in their study, the authors captured wild birds, and compared the behavior of infected and uninfected birds, as well as a number of physiological measurements. A quick summary of the results: Infected males were more likely to problem solve (in this case pulling a lever to release food) than uninfected males, but infected females were less likely to problem solve than their uninfected counterparts. Infected females were more exploratory (exploration of a novel room) than uninfected females, but infection did not influence male exploratory behavior. Infected males were more risk averse (retreating from a disturbance – noise caused by stick movement) than uninfected males, but infection did not affect females.

What does all this mean, exactly? Well, one of two things: One, males who get infected differ from females who get infected. Or two, infection changes the behavior of males and females differently. The first scenario argues that infection does not change behavior, that certain behaviors instead make individuals more or less likely to become infected. According to Dunn et al. (2011), for example, problem solving males should be more adept at using different food resources, and exposure to those different food resources should expose the birds to more parasites than males who are less capable at problem solving and therefore use fewer food resource types. The second scenario asserts that infection itself changes behavior, either as a host response to the parasite or direct manipulation by the parasite. While one can generally use information about the biological system to hypothesize whether behavior causes infection or vice versa, the truly definitive way to test this question would be to do controlled infections and monitor behavior before and after infection.

Such distinctions, as well as male vs. female behavioral differences, can be important for a number of reasons. They might, for instance, affect species management programs. If one had a species infected with a parasite, and one thought that bold individuals were more likely to acquire and spread that parasite, one might imagine a culling or vaccination program that focused on bold individuals to decrease future parasite transmission. However, if infection makes individuals bold, this program could be relatively pointless. If one of the two sexes, moreover, is predominantly responsible for transmission of the parasite, one might focus isolation, vaccination, or culling efforts on that sex. One could probably list many other examples in which sex differences and the direction of causality in behavior-infection connections matter.

Or, one could end the blog. To finish, then: Sex matters.

Citations

Dunn, J.C., Cole, E.F. & Quinn, J.L. (2011). Personality and parasites: sex-dependent associations between avian malaria infection and multiple behavioural traits. Behavioral Ecology and Sociobiology, 65, 1459-1471.

Parasites and the Benficial Predator?

Parasites and predators, generally speaking, negatively affect the organisms that they use (i.e., parasites hurt their hosts, and predators are obviously deleterious for prey). However, as I mentioned in the last blog, in ecology everything depends (on the details). Here, I will focus on some of the complications that can arise when one considers the effects of parasites and predators together.

First off, parasites can be eaten. They can be eaten when they are inside a host, and that consumption can put the parasites in the right or wrong host (the right host would be the one in which the parasite can complete its life cycle). For example, improperly cooked pork can contain parasites (e.g., Taenia solium). These parasites do not “want” to get into humans; they cannot complete their life cycles inside humans, and instead tend to cause huge problems. Parasites can also be eaten when they are outside the host. Many parasites have free-living stages in the environment, and they need to be consumed in order to continue their life cycle. Such consumption can also lead the parasite to the right or wrong host (Johnson et al. 2010).

Both of the above consumptive scenarios (a parasite being eaten when it is in or outside of the host) contribute to parasite population dynamics (how large is the parasite population, how many hosts are infected, what proportion of hosts is infected). One could thus imagine that predation could facilitate or hinder parasite transmission. For instance, if hosts acquire more energy from eating parasite-infected prey than they lose from the infection, hosts might do better if they ate parasite-infected prey, and therefore predation could increase parasite transmission. But if non-host predators eat parasites in the environment or prey with parasites, then these predators might reduce transmission to the host species (Johnson et al. 2010, Lafferty & Morris 1996).

Importantly, predators also affect their prey by more than just killing the prey. As any hunter can tell you, prey tend to run or fight back when encountered with a predator. If prey survive a predation attempt, they tend to alter their behavior to reduce predation risk (e.g., increase hiding time and reduce foraging time). Such behavioral changes can happen even if the prey never experienced a direct predator attack. Simply exposure to the smell/sight/etc. of a predator, or the smell/vision/etc. of other dead prey, can elicit behavioral changes in prey. These behavioral changes may also affect that prey’s exposure to parasites. If, for example, prey are more likely to encounter parasites by staying in one place and reducing activity, predators may indirectly increase parasitism among prey. The opposite may occur, however, if prey activity increases exposure to parasites.

In a recently published paper, a group of authors attempted to discern whether the combination of these factors – predators eating parasites and predator effects on host behavior – sum to positively or negatively affect parasite transmission to hosts. Orlofske et al. (2014) found that in the presence of a predator (a dragonfly larvae), tadpoles reduced activity and acquired more parasites. Other authors have previously demonstrated that active tadpoles acquire fewer parasites than anesthetized tadpoles, so activity was the key factor driving the increase in parasitism in this study. Interestingly however, the authors also discovered that the purported predator (damselfly larvae) of the free-living form of the parasite in question (a trematode) did not actually eat the parasite in a more realistic experimental setting (but it did in previous laboratory studies). Further, damselfly larvae caused the same reduction in activity among the tadpoles as the dragonfly larvae, even though the damselflies are not predators of the tadpoles.

\While this study did not reveal that parasite predators reduce infection intensity (contrary to expectation), it did validate the idea that host predators should be expected to increase parasitism when predator behavioral responses work against anti-parasite behaviors. It also highlights the notion that everything in ecology depends on the details, and concepts that bear fruit in lab settings may not do so in the field for a variety of reasons.

 

Citations

Orlofske, S.A., Jadin, R.C., Hoverman, J.T. & Johnson, P.T.J. (2014). Predation and disease: understanding the effects of predators at several trophic levels on pathogen transmission. Freshwater Biology 59(5): 1064–1075

Johnson, P.T.J., Dobson, A., Lafferty, K.D., Marcogliese, D.J., Memmott, J., Orlofske, S.A., Poulin, R., & Thieltges, D.W. (2010). When parasites become prey: ecological and epidemiological significance of eating parasites. Trends in Ecology and Evolution 25(6): 362-371

Lafferty, K.D. & Morris, A.K. (1996). Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77:1390-1397.

Tradeoffs. Should you wash your hands?

 Last time, I wrote about the somewhat controversial topic of “borrowing” your co-worker’s food. The choice to steal involves costs and benefits: the energy you gain from that food vs. the costs may you suffer from stealing. This is a general example of a tradeoff: You cannot be both good at stealing your co-worker’s food and in your co-worker’s good graces.

Tradeoffs come in all forms. For example, I often hear the following proverbial tradeoff for humans: “Jack of all trades, master of none.” If you’re okay at everything, you are not likely going to be great at any one thing. At its most basic level, this tradeoff involves investment. How much energy should you invest in one activity over another? Many tradeoffs involve investment. Though humans can reproduce as teenagers, many wait to reproduce until after they have stopped developing (e.g., mid-twenties). Such a choice, while for many occurs for social reasons, also exemplifies the tradeoff between investment in growth or reproduction (should I reproduce now and risk being unable to take care of my children because I’m not big and strong, or wait until I can take care of them but risk losing the opportunity to reproduce?). Information gathering can also be a tradeoff. Do you buy products spur of the moment, or carefully research? In this situation, you are trading off time and energy. If you research, you are using your time and mental energies when they could be used elsewhere. If you don’t research, you might pay too much, buy the wrong item, or be more likely to return the item later.

While these examples focus on people, all organisms face tradeoffs, many of which markedly resemble the ones above. Many non-human animals, for instance, feed on multiple items. The animal can thus choose between specializing on a particular food item or generalizing to eat everything. If the animal specializes, presumably it will become better at getting that item or getting more energy from that item. If the animal generalizes, it will have access to a greater variety of food, but may not get as much energy out of that food. This is analogous to the “Jack of all trades, master of none,” idea above in that you can be excellent at eating one thing, or good at eating everything, but not excellent at everything. Animals may also experience tradeoffs with responses to natural enemies, where “natural enemies” refers to predators and parasites. For example, hosts are exposed to many types of parasites throughout their lives, and hosts may invoke different defenses against those parasites. Hosts may therefore experience tradeoffs between different defense mechanisms (investing in behavioral defenses may mean less energy for immune defenses) or tradeoffs between the different types of parasites (being good against parasite A may preclude defense against B).

Such tradeoffs may make it appear that organisms are inappropriately adapted to their environments. “Why does that host suffer so much damage from that parasite?” However, such judgments need to account for the overall environment of the organism in question. Perhaps an organism is poorly adapted to a parasite because the parasite does not infect that many hosts in the population, and food shortage is far more important for survival to the host? If that is the case, the host may favor food acquisition at the cost of parasite defense capability. Additionally, if a host displays poor immunity, perhaps it exhibits numerous behavioral defenses? Such tradeoffs and environmental details, importantly, may make it appear that a host is acting maladaptively (i.e., in a manner that negatively impacts its survival and reproduction). To illustrate, have you ever touched a doorknob? And then ate something without washing your hands? Someone might be able to argue that this was “risky,” or even maladaptive, behavior because it exposed you unnecessarily to potential infectious agents. However, it’s a tradeoff. How much time and energy would you be wasting by washing your hands, or how much would you be damaging your hands by exposing them to basic chemicals, vs. the likelihood that you will get sick if you do not wash your hands? To really evaluate this scenario, we need to know more about the costs and benefits of washing your hands. Maybe in your culture, hand washing is considered unattractive, and so you are more likely to find a partner if you do not wash your hands, making hand washing maladaptive. Thus, the take home point: As is often the case in ecology, everything depends (on the details).

 

Untitled

Hands are hard to draw.

Should you steal your (sick) co-worker’s food?

Do you have a co-worker, friend, or roommate? If you do, have you ever been in a position to “borrow” that person’s food? Did you? Ethical dilemmas aside, did you consider whether said person was sick?

Let’s say I have a co-worker named Gunter. If I take Gunter’s lunch, I will benefit from acquiring a “free lunch.” However, I might suffer costs if Gunter discovers who took his lunch. When I decide whether to purloin Gunter’s food, therefore, I am conducting a cost-benefit analysis. An additional factor I might include in this analysis could be whether Gunter is sick. If Gunter is sick, for example, I might risk acquiring his infection by eating his food. Such infection would likely more than negate the benefits I obtained from eating Gunter’s food. Gunter’s sickness would consequently dissuade me from “borrowing” his food. But, what if from past experience I know that Gunter gets incredibly angry when anyone borrows his food – except when he is sick. Naturally, he is more displeased about losing his lunch when he is sick than when he is healthy, but when he is sick he doesn’t have the energy to confront anyone about the loss. And now I have a conundrum. I am likely to suffer negative consequences from a healthy Gunter if I am discovered with his lunch. I may also acquire an infection from Gunter if I take his lunch when he is sick. But I am less likely to suffer negative consequences from Gunter at that time, even if I am discovered. So should I steal Gunter’s lunch, and when?

Unfortunately, no simple answer exists for this situation. The answer all depends on the cost:benefit ratio – the benefits I get from Gunter’s food relative to the costs I may suffer from stealing. If benefits are high enough, it would be optimal for me to steal all the time, regardless of Gunter’s state. If benefits are high, but costs due to Gunter’s behavioral response are high, it might only be optimal for me to steal when Gunter is sick.

If you think this example is a little contrived, well, you’re right. But not so much as you might think. For instance, Bouwman and Hawley (2010) discovered that male house finches preferentially fed near males who were infected with a bacterial parasite (mycoplasma), even though feeding sites enabled high transmission rates of the parasite. Bouwman and Hawley also noted that infected males were less aggressive than uninfected males. The authors therefore concluded that males who fed near an infected male benefited from encountering less aggressive males (meaning the former males were more likely to be able to feed without incident). This benefit might or might not outweigh the costs of infection for the population as a whole, but at least at the individual level, benefits appeared to override the consequences.

This house finch result has interesting implications for the evolution of host-parasite interactions. We often think of hosts evolving to maximize fitness, which means reducing parasite costs to an absolute minimum, but this does not have to come from reducing parasite infection to a minimum. If you engage in behaviors that lead to infection, but you get more benefits from those behaviors than the costs of infection, selection will favor that behavior, even though it increases infection.

 

Citations

Bouwman, K. M., and D. M. Hawley. 2010. Sickness behaviour acting as an evolutionary trap? Male house finches preferentially feed near diseased conspecifics. Biology Letters 6:462-465.

Does your behavior influence your immune system?

I previously wrote an article about how behavior can influence transmission. In that piece, I focused on behaviors that can increase transmission (in some cases, bolder individuals can be more likely to contract a particular parasite because their boldness may lead them to make risky decisions, such as fighting with infected individuals). However, to provide a fuller picture of host behavior in parasite transmission dynamics, I decided that I should now talk about how behaviors can influence parasite infection in a way that benefits the host.

I cannot speak with authority for disease ecologists as a group, but generally speaking I think we all realize that host behavior is very important for parasite transmission. Unfortunately, the effects of behavior can be very hard to quantify. Even in systems in which behavior and parasite transmission can be linked, demonstrating causality becomes incredibly difficult. For example, in my earlier post on boldness and parasite transmission, Dizney and Dearing (2013) could not determine whether infection caused the boldness, or whether boldness determined infection. It seemed likely that boldness was influencing infection given the biology of the system, but this inference was by no means proven beyond all doubt. Thankfully, such hindrances are not universal.

Daly and Johnson (2011), for instance, performed simple, yet elegant experiments with tadpoles. By comparing the number of infections anesthetized tadpoles and regular tadpoles received, the authors elucidated the effect of tadpole behavior on parasite infection (the authors had shown previously that anesthesia does not affect tadpole physiology or immunity). Anesthetized tadpoles had a much greater number of parasites (in this case trematodes) than the control tadpoles, demonstrating that tadpole behavior protected the tadpoles from infection. Expanding upon these results, another group determined that tadpole behavior also influenced the location of the parasite infections (Sears et al. 2013). Anesthetized tadpoles sustained the majority of their infections in the head, while untreated tadpoles suffered them in the tail. As one might imagine, parasites in the brain are a much more serious infection than in the tail, especially because these tadpoles lose their tails in the course of their development. Thus, tadpole behavior not only reduced the number of infections the tadpoles suffered, but also shunted the infections that they did receive to less critical areas.

If these examples seem a tad different from any human disease (who has heard of someone being able to control whether a cold causes headaches or congestion), house finches may provide a more relevant example. Recent work with house finches has demonstrated a number of interesting correlations among behavior, infection status, and the immune system. For example, in a study testing house finch preference to associate with a sick or healthy bird, house finch males chose to associate with a healthy male more than a sick one, and males that were closer to the sick bird invested more in immune defense than finches that chose to be farther away (Zylberberg et al. 2013). In another house finch study, similarly, male birds that invested more in surveillance behaviors (which are thought to reduce parasite exposure because the finch would not be blindly entering a novel area or eating a novel food) invested less in immune defense. Furthermore, as male avoidance of novelty decreased, investment in immunity increased (Zylberberg et al. 2014). Thus, house finch males appear to balance investment in anti-parasite immunity and behavior – as investment in behavioral defenses increase, immunity declines, and vice versa. These results may be more applicable to humans in that while we cannot control where a parasite infects us (as far as I know), we can perform behaviors akin to the house finches: We can control whether we choose to go to work when we are sick, or how much we wash our hands, or whether we eat food off the floor (e.g., “the 10 second rule”). It remains unknown whether such behaviors, or lack thereof, correlate with the immune system in humans as they do in house finches. If they do, the next question becomes “why?” Why should some individuals invest in behavior and others the immune system? Do individuals differ at birth or during childhood in some way that set them on a behavior or immune system course? Are these differences selectively favored? Perhaps a population with mixed defense strategies survives better through time than one in which all individuals use the same parasite defense strategy? Perhaps things to think about the next time you are debating whether the 10 or 30 second rule applies.

Citations

Daly, E. W., and P. T. J. Johnson. 2011. Beyond immunity: quantifying the effects of host anti-parasite behavior on parasite transmission. Oecologia 165:1043-1050.

Dizney, L., and M. D. Dearing. 2013. The role of behavioural heterogeneity on infection patterns: implications for pathogen transmission. Anim Behav 86.

Sears, B. F., P. W. Snyder, and J. R. Rohr. 2013. Infection deflection: hosts control parasite location with behaviour to improve tolerance. Proceedings of the Royal Society B-Biological Sciences 280:5.

Zylberberg, M., K. C. Klasing, and T. P. Hahn. 2013. House finches (Carpodacus mexicanus) balance investment in behavioral and immunological defenses against pathogens. Integrative and Comparative Biology 53:E400.

Zylberberg, M., K. C. Klasing, and T. P. Hahn. 2014. In house finches, Haemorhous mexicanus, risk takers invest more in innate immune function. Animal Behaviour 89:115-122.