In this podcast for Functional Ecology, Assistant Editor, Frank Harris, sits down with Lauren Nadler and Sandra Binning—two of the four guest editors (also Shelley Adamo & Dana Hawley)—to discuss the recently published cross-journal (with Journal of Animal Ecology) Special Feature titled, The Mechanisms and Consequences of Infection-Induced Phenotypes.
This special feature highlights recent insights into the ways parasites alter host phenotypes across a range of systems. Here, we contextualize how each contribution expands our knowledge of the role of parasites in driving individual variation in animal phenotypes.
Useful links
Some other blogs on parasites and disease ecology:
While not exclusively parasite/disease content, these science-focused pages are excellent:
Some parasite-focused societies:
Transcript
Frank: Today, I’m delighted to welcome Lauren Nadler and Sandra Binning to the podcast. Laura and Sandra make up 2 of the 4 guest editors on Functional Ecology’s cross journal SF with Journal of Animal Ecology: Mechanisms and consequences of infection-induced phenotypes. The other two guest editors who weren’t able to join us today are Dana Hawley and Shelley Adamo.
This cross-journal special feature is due to be published in April 2023. It aims to bring together biologists working on a wide range of host-parasite systems and topics in order to synthesise our current understanding of host-parasite relationships and brainstorm how to move the research area forward in an uncertain future.
But before we get into the special future, I think it would be good to do some introductions. So we’ll start with Lauren. Where are you from? What your research interests? And could you just tell us a little bit about your journey towards becoming an ecologist?
Lauren: Thanks for having us today. So I am originally from the US, but I’ve moved around a ton—I’ve done various parts of this academic journey in the UK, in Australia, in Norway, kind of all over. I always knew I wanted to work with marine organisms—I have wanted to be a marine biologist since I was five. I went to aquarium when I was five years old, and I was just captivated and thought it was the coolest thing I’d ever seen.
Bringing it forward to the present, my journey led me to pursuing a PhD in Australia, which is actually where I met Sandra—We were part of the same center of institutions. I was studying the behaviour and physiology of coral reef fish, specifically looking at how certain physiological mechanisms might promote social behaviour. And I was really interested mostly in the ecology at that point, although I had some interest in environmental disturbance. Then, as a postdoc, I learned that there was an opening to work on this host-parasite system in California at Scripps Institution of Oceanography. It was basically a parasite that was very different from anything I’d ever heard about before. It had three different hosts, it had to pass from snails to fish to birds, and there was all this literature about all the weird and funky ways that the parasite affected the behaviour of the fish. So I was really excited about this! There were some studies on how their physiology changed with the parasites, so it kind of fit into all of my interests from when I started as a PhD student, but with a focus on parasites.
Once I started this job, I realized the huge role that parasitology plays. There was a lot to learn and it was very exciting, but also a little overwhelming. Following this, Sandra and I both ended up kind of working on similar ideas, but this was after we both had left Australia. We both got to be really interested in this idea of how parasites alter their hosts, and how different kinds of parasites may have different impacts on their hosts. Learning about this has been really interesting and this has brought us to where we are today.
Frank: So can I ask just quickly, with regards to marine biology, are there any differences between your idea of it growing up and the reality of actually doing it as an adult? I’m just thinking that most of us grow up watching Blue Planet and seeing all of these beautiful, larger than life creatures… And then you’re just studying plankton. Not that that’s not interesting, might I add, but I was wondering if you could touch on the idea vs the reality of it?
Lauren: Definitely! Five-year-old me was really into marine biology because they had touch tanks at the aquarium. So I got to touch sharks and all these different creatures. My grand plan, at that age, was that I was going to have touch tanks as a grown up! I didn’t understand that this wasn’t a job. I started out being really interested in these charismatic megafauna—they’re the cute and cuddly creatures like whales and sharks… Maybe sharks… And turtles and animals like that. But I think as I got more interested in science, I became really interested in being able to conduct experiments, so actually being able to manipulate things and pinpoint the causal mechanisms behind the things that I was seeing. So, because I very quickly found out that it’s actually really hard to keep those charismatic megafauna in a controlled lab setting, I started working with really small fish. These aren’t necessarily beautiful for a lay person, but I think they’re cute! I think it’s definitely evolved, and what I’ve been interested in and my understanding of the job has also evolved through time. Over time, I became more excited in some of the smaller things that have really big consequences for all of those bigger things that I used to be so excited about.
Frank: Wonderful. I’ll pass the ball over to you, Sandra.
Sandra: Thanks a lot, it’s great to be here! It’s so nice to be able to talk about this and we have really appreciated the opportunity to work with all of you and get this thing over the line!
So I’m based in Montreal and I’m originally from Montreal, Canada. But, like Lauren, I have really moved around a lot over the course of my career. I also did my PhD in Australia, and as Lauren mentioned, that’s where we first met. I did a postdoc in Switzerland afterwards and have done field work all over the world. I am also mostly focused on marine organisms, although I now also work on freshwater stuff, so I’m definitively an aquatic person—no bias in terms of salt- and fresh-water!
Kind of like Lauren said, the way I got into specifically working on parasites, which is what my current lab at University of Montreal really focuses on, was studying the physiology, behaviour and ecology, of infected fishes, mostly. But I really got into parasites and the role that they can play in the ecology of hosts completely by accident—it wasn’t something I set out to do. My PhD was also focused on coral reef fish and physiology related to waves, water motion, and how the exercise abilities of fish in really wave-driven environments varied across different habitats. However, while I was swimming and snorkelling on the reefs, I just kept seeing these fish that had this huge parasite attached to the side of their heads and I got so obsessed with it! I was really thinking about kinematics, swimming in water and drag, and the difficulty of swimming in these environments, and these poor fish had this huge thing on the sides of their heads. I wondered, how are they able to deal with? So I sort of went off on this side project that had nothing to do with what I was originally supposed to be doing for my PhD and I was hooked!
I started really pursuing this again throughout my postdoc. I was able to work on a system of cleaner wrasse that were removing parasites from other fishes, which was a different take on the whole idea about parasite infection and host-parasite relationships, so that was super neat! I was also thinking about behaviour and how fish deal with infection and now we’re bringing some of these ideas back to Canada to try apply them to the freshwater systems that we are working on.
Frank: Fantastic. Right, bonus points if it’s a parasite, but what are your favourite study organisms?
Lauren: So mine is actually the fish I did my PhD work with. They are these small damselfish, the blue-green Chromis viridis. They are really easy to keep in the lab, and they’re really easy to catch. When they get used to being in the lab, they get to know when they’re going to be fed so they’ll come to the surface like puppies and splash you if you don’t feed them. I absolutely love them!
Sandra: I’m going to be different and say a parasite just for fun. I’ll probably say this big parasite I was talking about that hangs off the side of a fish’s head. They’re a genus called Anilocra and I guess you can think of as being similar to ticks, but ticks that stay on a fish for a really long time and they get super big! The females are the ones that have this marsupium which is like a little pouch in their abdomen where they have little babies, and if you take them off you see these little babies swimming out—they’re super cool. They look a bit gross, but I really love them. There’s a whole bunch of different species in lots of different fish. You can find them in the Caribbean, in the Indo-Pacific—you can find them just about everywhere, so that’s my favourite genus of parasite.
Frank: So before we go into the special feature, I always like the idea of setting things to right. I know that sometimes the idea of something, as we spoke about with marine biology before, can be very different to the reality in scientific terms. So with that in mind, is there anything that you can think of with regards to host-parasite dynamics and interactions? Something that you could share with the listeners that could be very interesting and perhaps change their perspective on the subject? Most people probably just think parasites are gross and that they are terrible for their poor hosts, but I know the dynamics don’t work exactly in that way.
Sandra: Parasites are so complex—that’s one thing that a lot of people don’t realize. When we say parasite, we’re really talking about any organism that extracts resources from another organism, at a cost to that other organism (the host). That encompasses such a huge range of different types of organisms. When we think of parasites, we might think about things like tapeworms or, again, ticks like I mentioned before. We think of things that are bad for us, but there there’s such a wide range of animals, and also bacteria that have these parasitic relationships.
I think that that is one thing that a lot of people are surprised about—how diverse this category of animals and organisms actually is! Additionally, as Lauren mentioned before, the fact that some of these organisms have extremely complex life cycles where they sometimes need two, three, or even four hosts to be able to complete their life cycle. They have very specific things that they do and need from each of these hosts. I think that level of complexity just blows people’s minds. When I talk to my students about it, it’s really something that they don’t think about when observing ‘simple’ organisms like little worms. They don’t think about the fact that they can have these really incredibly complex ecologies and life histories. I think that is really, really fascinating if you’re interested in the natural world and how things evolve.
Frank: Thank you for that answer, Sandra. Now we’ll pass on to Lauren to tell us some interesting facts about host-parasite dynamics that we might not be aware of.
Lauren: The thing that I have found most interesting is the fact that most of us assume that parasites are gross and that we don’t have them. But actually, in reality, we all have lots of parasites—all animals probably have several parasites. There was an interesting quote that I had heard—I don’t remember who said it and I probably won’t say it accurately—”tell me what parasites you have and I’ll tell you who you are.” The reason that this quote is so relevant is that what parasites we have are going to depend on our unique history, who we’ve interacted with, where we’ve lived, what we’ve eaten, etc. Every person is unique, not just in their own combination of traits, but one of those interesting traits is what parasites they have and the way that they have lived their lives.
Frank: So I think that’s a good point for us to actually start talking about the special feature. So I will ask Sandra to, in plain terms, explain the novelty of this special feature and what it contributes to our understanding of the mechanisms of infection-induced phenotypes?
Sandra: So we’re not the first people to think about parasites. I mean, people have been researching parasites and their hosts for centuries! I want to make it clear that we’re not completely reinventing the wheel here. However, the thing that is really novel and exciting about this special feature is that we’re really trying to approach this relationship between hosts and parasites from multiple different angles.
We’re really looking at it from all different levels of organization. We have authors who are thinking about these interactions at the level of what’s happening in the cells. We also have authors thinking about what’s happening in the organism, but with a very mechanistic analysis of how these parasites are really going about changing things in the host at a cellular level. We have people who are approaching it from the perspective of the host, so, at an individual level, what are the types of changes and how does infection impact interactions that an organism is going to have with other organisms. We also have studies that are scaling up to the level of ecosystems, i.e, what are the broader scale impacts of infection on communities and processes that are happening in the ecosystem. So we’ve really tried to take this multi-scale approach. We are also looking at different types of ways that parasites can impact hosts. Again, we often think of parasites, by definition, as being bad for hosts; however, the ways that a parasite impacts a host’s movement or physiology or behaviour is not always something that can be described as ‘causing damage’. Some of the changes that we’ve seen in hosts is from the host trying to change its behaviour to minimize the cost of the parasite. There’s lots of different ways that the interaction between host and parasite can affect physiology, behaviour, and ecology. And so we’re really trying to bring all of these different things together and synthesize in order to see what commonalities jump out, across different scales and across different mechanisms. I think that is the really exciting and novel aspect of our special feature.
Frank: Thank you. I’ll pass on to Lauren to take the baton forward and talk about some key takeaways, maybe some interesting results?
Lauren: I think Sandra summarized it really well. What we were really interested in doing is taking researchers, for one thing, out of their own individual system. Whether they work on insects or mammals or fish, we really want them to think about what they are learning in a study system and how could it be applied to other systems. Are there some general ideas that we can think about and learn from by looking across these different animals?
I think there are some misconceptions about how parasites interact with their hosts. There are things, for those of us working intensively in this specific field, we know about. But we were trying to think about how these ideas can be expanded to folks that aren’t necessarily working on host-parasite interactions. When you’re just looking at the ecology of how the animal lives in an environment, you want to work on the healthiest animals, and if you see an animal that has a big parasite—like the one Sandra worked on in the past—you might potentially exclude it from your study. This is not the most realistic way to help us understand how animals live in nature. We want to share ideas and make them accessible to folks that study areas that seem completely separate from parasites. We want them start to think about how parasites, in the environment of the animals they study, might impact the principles that they focus or work on. Doing this will mean we can expand these ideas and help people to think more universally about how parasites may be impacting the types of processes that they are studying.
Frank: That’s remarkable. So both of you have papers that you’ve authored which are part of this special feature. Perhaps you can talk a bit about your contributions in those papers?
Sandra: I’m really excited about the contribution from my group. I would like to give a shout out because my contribution, I should say, was very small to the paper—it was really driven by the graduate and undergraduate students, both in my lab and also in a couple of other labs. This paper was basically a pandemic project. In the fall of 2020 a lot of my students completely lost their field seasons—we had very, very strict lockdowns here in Quebec so we weren’t allowed to do very much field work and the students were really quite worried about it. One of my students, Jérémy De Bonville, who is a PhD student in my lab had this idea about doing a collaborative literature search, and we asked the following questions: how might parasites be impacting host phenotypes, especially related to physiology and behaviour?; and how much are other people—who are working on questions related to animal performance—thinking about the impacts that parasites might have on their study systems?
I thought these were such cool questions that really lent themselves well to the pandemic where everyone was stuck at home and couldn’t do field work. We got together different PhD students and undergrads, as well as graduate students from other labs who were working on different systems. We all came together on gather.town which was a platform we used for work sessions where everyone was systematically performing this research. I have to reiterate, this was completely driven by the graduate students! I think it came together really nice and I’m really, really proud of the work that they’ve done. To have it featured in this special feature is really the cherry on top! They really helped to turn a bad situation into something that was productive for everyone.
Frank: I’ll ask the same of Lauren.
Lauren: So I am a co-author on one of the contributions to this special feature. This paper was led by Marco Vindas and it came out of my post-doc in Norway. We were looking at the effects of a tiny intracellular parasite on some of the model fish species that are used in biomedical studies. We’d already done some work with zebrafish, so we decided to see if there were similar impacts on medaka (Japanese rice fish/Oryzias latipes), which are another commonly used model fish species. There was one study that showed that if you house infected zebrafish with this intracellular parasite with medaka, the medaka would become infected and you have this infection that gets passed back and forth between multiple species.
So with the same procedure we had used in the past on zebrafish, we used the same method with medaka and gave them a lot of parasites—I mean a lot, a lot, a lot of parasites—and we were baffled when we could not detect infection in the medaka in spite of the that fact that we spent so much effort and time trying to infect these fish. One of the most important issues in our field is understanding the difference between whether a host is susceptible to the parasite, whether it is resistant to it, or whether it is tolerant of it. Therefore, not detecting an infection doesn’t necessarily mean that the parasite hasn’t gotten in and made all of these effects on the host, because, potentially, the host was just really good at fighting off the parasite when it was trying to get in. However, that fight is actually extremely costly for the host. It takes a ton of resources, especially when they’ve fought it as successfully as these fish have. Because we know these fish were exposed to a ton of parasites that, in the past in other studies, they’ve been shown to be susceptible to, we wanted to explore whether exposure might affect their behaviour. Were they behaving differently in the longer term after this parasite exposure, even though they never actually got an established infection?
What this study showed is that the behavioural differences were actually really strong between the two study species. There were potentially changes in activity, in sociability, in aggression—all of these different aspects of their behaviour were different if they previously had exposure to parasites. This result really does upend what we think about in terms of infection. We think about the parasites that we find in our hosts; however, we have no idea—especially when we study wild animals—what parasites they’ve potentially been exposed to—but successfully fought off—in their environment, and what the implications are for that battle between hosts and parasites because of how costly it is to actually fight them off. What we ultimately showed in this study is that even in hosts that were really good at resisting parasites, the cost of fighting infection does have longer term impacts on behaviour.
Frank: That’s remarkable. I know in your editorial you mentioned how, under climate change scenarios, we need to know how animal phenology is changing. Therefore, I’d like to ask, and I’ll start with you, Sandra, where should research on parasite-host dynamics and general ecological research be directed towards next and what changes do you hope this special feature will precipitate in the field?
Sandra: Well, this is just my humble opinion. Of course, people have different opinions on this because it’s a massive question. I think that what we’re hoping to do with this special feature is to get people who don’t typically think about parasites to at least acknowledge their existence and the impact that they might have on their study system(s). We want people to try to bring a little bit more of that ‘ecological realism’ back into their own work, because, whether we like it or not—or even whether we’re interested in it or not—most wild animals do have parasites and they can have pretty big impacts on the performance of the animals that we are trying to study. If we ignore parasites, we’re potentially losing a key piece of information, and, again, just thinking about the idea that animals have to adapt to life and reality in nature where there are parasites and infections everywhere—we’ve had to do that with COVID! It’s something that we are constantly having to deal with in our natural environment. So this is something that I’m hoping people are going to increasingly become more aware of. We want people to think about how these host-parasite interactions are impacting the types of questions and research that we’re doing. Thinking forward, I want to bring attention to the idea of co-infections—that you can have more than one type of parasite, more than one species, more than one individual parasite, more than one parasite at different life stages, and in all of these instances there are different effects on the hosts. These interactions are inherently complex, but we should embrace that complexity as opposed to ignoring it. I think it’s something that is really interesting and something that will really help us to better understand how organisms are going to be potentially affected by other types of stressors such as climate change. If we’re interested in climate change effects on wild animals, we should also be interested in how climate change might be affecting host-parasite interactions, because those interactions cannot be dissociated.
Frank: Fantastic. And Lauren?
Lauren: I think Sandra has summarized it really well. I think these are inherently very complex interactions and there’s a lot that we don’t know, partially because it is really difficult to study these ideas in the exact way that they occur in nature. Furthermore, it’s difficult to study more than one parasite at one time; however, some of the papers in this special feature have done a really amazing job of starting to really get at that complexity. Hopefully, we can create a structure that others can follow to potentially tackle what are very difficult questions. Readers should be looking at what these papers have done so that they can generate ideas about how they could potentially utilise these ideas in their study systems.
Frank: So as we begin wrapping up, I think it’s always good to take stock. This is your opportunity to give a shout out to groups and people who helped along the way!
Sandra: Well, I think we would be amiss if we didn’t acknowledge Shelly Adamo and Dana Hawley for helping us to put this special feature together. Shelly is someone who we interacted with at conferences in the past—the idea for this special feature came through conference discussion! Dana is someone who was brought on board via Shelly, so Lauren and I, rather amazingly, have never actually met Dana in person! We’ve interacted with her so much through putting this special feature together. Maybe this is one of the wonderful things that has come out of the pandemic—it’s now so much easier for people with the resources and know-how for online collaborations to put things together!
I also want to thank all the contributors to this special feature. People were very excited to contribute their work. The process of getting people to be on time and respect the deadlines, and really put a lot of effort into the revisions was truly remarkable. I think that the success of this special feature is of course directly related to the authors who’ve contributed. A massive thanks to everyone who contributed and made this special feature possible.
Frank: Amazing. I know Lauren there’s a lot of shoutouts there, but is there anyone else to add to that?
Lauren: Of course! Thank you, Frank and Kirsty Scandrett for helping us to get all of these papers over the line from the editorial side. We’re super appreciative of all of your help and advice, especially because Sandra and I had never organized a special feature before!
I think one thing to mention is that this special feature partially came out of Sandra and I talking at the Society for Experimental Biology Annual Meeting a couple of years running. Further to our chats, we also ran sessions there which helped hone these ideas, so I wanted to give a shoutout to SEB! Lots of the discussions about these ideas happened during that meeting, so it’s nice that we are able to get back to in-person meetings where these sorts of casual conversations are starting up again.
Frank: So that actually brings everything together quite nicely for the last question that I’d like to ask. It’s a two-parter this time, because we’re talking about special features. The first one is: what advice would you give to your younger self, going through all the ecology madness of PhD life, and what advice would you give people that might be interested in running a special feature? To fire back the compliments, I must tell our listeners that this has been an absolute clinic on how to run a special feature. We couldn’t be more pleased with the interaction that we have had and the buy. Every single point has been kept perfectly in terms of timing and it’s just been a delight to work on.
I’ll stop rambling. So, advice to yourself and advice to others who might be interested in running a special feature. I will keep it to one piece of advice so that we can’t tread on each other’s toes. Let’s start with Sandra.
Sandra: Thank you for those kind words, Frank. It’s really nice to hear. Sometimes, Lauren and I felt like we were running a little bit in the dark, so I’m glad that it all came together so nicely! Advice to myself when I was younger… I guess I would tell myself to just do what you want and do what interests you. Make sure that you’re driven by your passions. I, like I said, I never set out to do a PhD that had anything to do with parasites, and look where that exploration of my interests has taken me! I would say don’t be afraid of following your passion and doing something that’s a little bit outside of your wheelhouse! For advice on putting together a special feature, get a great team of editors together! Lauren and I were able to bring Shelley and Dana in, and their insights were really critical in making sure that everything worked smoothly. Once you have your core team together, if you have a good way of working then the rest will fall into place.
Frank: Perfect. And Lauren?
Lauren: In terms of the one thing I would tell my younger self or younger folks, I do have one piece of great advice I was given during my PhD. When someone is doing a PhD, there’s a lot of noise with people saying “you’re doing this stuff but you should be doing this and you should be accomplishing that.” It can become very stressful if you get locked into a cycle of thinking ‘I should be at a certain place and I’m not there yet’. The best thing is just to do things that you’re interested and that you’re excited about. I think that will ensure that you enjoy your job, because this can be a really fun and fortunate position to be in, to just delve into interesting parts of science… So, focus on what you’re interested in and kind of just forget the noise. Stop thinking about what you should do—this “should’ve, could’ve, would’ve’—and just do what you’re passionate about.
In terms of what I would say about the question about special features, I think one of the great parts of this process has been the ability to just reach out to people whose papers I’ve thought were really interesting! I think reaching out to people that you don’t know and not just sticking within your network is a great strategy because then you can expand and think about things outside of your particular narrow viewpoint. It’s an opportunity to talk to people who you’ve never had the opportunity to get in touch with, perhaps at a conference or something. We were really amazed with how interested people were, that we had never met, in contributing to this special feature, so I think just networking and reaching out to people is a great thing to do if you want to create a special feature.
Frank: With conference season coming up, I imagine that’s a great place to recruit as many people as possible for any projects! I just want to thank both of you and the other two guest editors, Dana and Shelley. This special feature will be available in early-April 2023.
