Special Report: #NZASP15 Part II: Ups and downs of shark parasites, networks, and Toxoplasma gondii

This is Part 2 of my report on the joint annual meeting for the New Zealand Society of Parasitology (NZSP) and Australian Society for Parasitology (ASP) in Auckland, New Zealand (#NZASP 2015), which I attended earlier this month. If you had missed Part 1 of my report, you can read it here.

#SharkSelfie

My previous post ended on a note about shark tapeworms, so I thought we should start this one off on the same note. In the previous post, it was established that the giant squid (at least in its juvenile form) is a part of some shark's diet, and is thus used by some tapeworms to reach their shark host. The talk by Trent Rasmussen from Otago University further expands on the role played by such prey items in determining the tapeworm community of sharks.

The parasite fauna of any given species is governed by a wide range of different factors. For tapeworms in sharks, a previous study showed that body size and depth range were good predictors for the diversity of tapeworms found in any given shark species. Trent's study expand upon that by including dietary range as an additional factor, and found that while body size and depth range were good predictors for tapeworm diversity, diet breadth - or the diversity of prey consumed by the said host shark - was an even better indicator.  With each type of prey harbouring different types of tapeworm larvae, having a varied diet is a great way to acquire an eclectic set of parasites. It seems that for sharks, your tapeworms are what you eat

Speaking of which, that leads into Robert Poulin's talk about the ups and downs of parasite life cycle. Many parasites have complex life cycles and have to go through many different animals in order to complete it. The problem with such a way of life is that there is massive attrition at each stage of the life cycle: for some parasites (like the tapeworms which infection sharks) they need their current host to be eaten by the next host to complete its life cycle (known as "trophically transmitted parasite"), and the likelihood that the parasitised prey will be eaten by the right predator species out of all the prey individuals in a population is very, very low. Given this cost, do such parasites have adaptations to offset the losses at each stage of their lives?

Digenean trematode cercariae
(free-swimming larvae)

That was the central question behind the study described in Robert's presentation, which he conducted with postdoctoral researcher Clément Lagrue and their team. From their study, it seems digenean trematodes (or flukes) seems to have evolved a key innovation that allows them to offset that some of that losses - and all it takes is the body of a snail at the first stage of their life cycle. The study itself was a massive undertaking which involved taking samples from four New Zealand lakes, at four different spots at each lake for a total of sixteen sites. At each of the site, they collected pretty much everything they could which added up over 650 thousand individuals animals, and they ended up dissecting over 400 thousand invertebrates and counted all the parasites that they found.

From this, they found that while was a reduction in the number of individuals for trophically transmitted parasites like tapeworms or roundworms, for digean flukes, there was actually an increase in the number of individuals in the population by two- to three-folds between their first host and the second host. Because flukes converts its first host, the snail, into a parasite clone factory, it is able to turn a single successful infection into thousands of infective larvae for the next step of their life cycle. The final stage of the life cycle of the fluke still involves being eaten by the right host, which means they are in the same boat as the tapeworms and roundworms, but at least they had been working with better odds than those other parasites.

Events like conferences are all about networking, but out in the wild amongst reptiles, "networking" is not so much about exchanging email and ideas as much as it is about exchanging parasites. Stephanie Godfrey from Murdoch University presented a talk about her research on how parasites can spread among social network in reptiles, and how models of such networks can be used to manage wildlife disease.

Photo by Caroline Wohlfei

One of the study she described involved testing the prediction strength of different epidemiological models, using the parasite-host system of ticks on Sleepy lizards (Tiliqua rugosas). These lizards live in the semi-arid desert of outback Australia where there are few shelters for the ticks. In such habitats, the parasites have an infectious window of 11-24 days to hop on a lizard or they will they expire, so the bushes where such where lizards congregate and take shelter inadvertently become places for tick exchange. When the lizard stop at those sites, they drop off tick larvae which lay in wait for another host to come along. Her study was a mark recapture experiment which involved releasing two "pulses" of tick larvae with known genotypes to see where they end up.

She test the ability of three different types of models to predict how the ticks would spread in the lizard population; one based on (1) social network, another based on (2) spatial proximity, and finally one based simply on (3) lizard behaviour. It turns out that network model had the highest predictive power, but the spatial model was not far behind, and it also depended on whether it was modelling the first or second larval pulse; a variability which was most likely due to seasonal variations that affected tick larvae survival

Finally, I end this post with a note about Toxoplasma gondii - the famed rodent-whisperer. If there is ever a parasite that has captured the public's imagination, it is this one. In the eyes of most people, Toxoplasma gondii might as well be called "Deus ex Parasita" or "Plot Parasite" as it has been suggested as being responsible for everything from schizophrenia, to brain tumours, to influencing human culture and even for making the French so, well, French.

Is that a rodent I see before me?

But what is the basis behind this reputation? Amanda Worth and other scientists from Murdoch University have been questioning whether such behavioural alteration necessarily benefits the parasite. In contrast to the usual narrative, T. gondii seems to do really well without ever ending up in a feline - the cat can act as a site for sexual reproduction, but it seems T. gondii can get by perfectly fine with just asexual reproduction (for a full coverage of this, see this from the zombie ants blog here).

Additionally, studies which investigated the question of T. gondii host manipulation often do not take into account pre-existing behavioural difference between individual rodents. In her study, Amanda compared the behaviour of both uninfected and T. gondii-infected mice, and to control for within-species variations, she observed the behaviour of the experimental rodents both before and after exposure to the parasite. Her results were...well, not as clear-cut as the other studies may have made it out to be.

For example, she noticed that some mice already had preference for cat urine before they were exposed to T. gondii. And while the T. gondii-infected mice spent more time hanging out in the open, they did not show a particular preference for cat pee (in contrast to the usual narrative about T. gondii). In the non-exposed mice, individuals that are more bold also tend to be more active, thus these two behaviour seems to be linked. But in T. gondii-infected mice, those two behaviour are not as well connected. While uncoupling certain behaviours in some cases may render an animal more susceptible to its predator, but whether that would make a rodent more likely to be eaten by a cat is another question.

So it seems that in this particular study, the effect that the infamous T. gondii inflicted upon their rodents hosts is relatively limited. Maybe there are variations between different T. gondii strains in regards to their capacity for altering host behaviour. Studies on other parasites have shown that within a given species, individual parasites or strains are known to vary in their propensity for host manipulation. Either way, it seems that there is Toxoplasma gondii the parasitic organism,  and then there is Toxoplasma gondii - the near-mythical entity which exists in our collective imagination; a parasite which is capable of masterfully manipulating people's behaviour so that they will believe just about any story that has "cat parasite" in its headline.

Next month, it will be guest posts time on this blog and I will be posting the best student blog posts from the Evolutionary Parasitology class of 2015 - so be sure to stay tuned for that! Until then, you can check out some of the student blog posts from last year here.