In this podcast for Functional Ecology, Assistant Editor, Frank Harris, sits down with Thomas Chouvenc—Assistant Professor at the University of Florida—to discuss his recently published paper ‘Eusociality and the transition from biparental to alloparental care in termites.’

Thomas’ paper shows that, in eusocial insects, colony foundation is a critical bottleneck, where the founding individuals must engage in a temporary (but obligatory) parental care phase that may ultimately reflect on the family unit conditions of their sub-social ancestors.

Transcript

Frank: Today, I am very happy to be chatting with Thomas Chouvenc. Thomas is Assistant Professor of Urban Entomology at the University of Florida. His research focuses on subterranean termite biology, with a particular interest in the field of evolution of insect societies, termite ecology and termite control. He has authored 85+ papers and is also the organizer of the UF/IFAS School of Structural Fumigation, the Termite Course for Professionals, and the International Termite Course.

In addition to finding out more about the author himself, we are discussing his recently published research article: Eusociality and the transition from biparental to alloparental care in termites.

So hello Thomas, how are you?  

Thomas: Hello, Frank. Thanks for having me and I’m doing good.  

Frank: To kick things off, let’s do some introductions. I want to find out who you are, where you’re from and what your research interests are. 

Thomas: I’m Thomas Chouvenc and I am Assistant Professor at the University of Florida, and I study termites. I’ve been studying termites actually for the entirety of my adult life—it’s been about 24 years now. I grew up in a small village in France and, from a young age, I was exposed to nature and bugs—as a young kid I was always looking at ants and beetles and creepy crawlers. I got interested in a book about the biology of ants which showed how this little creature—so simple at a glance—is very complex, well-organized, and successful. This early fascination directed me to go for a biological degree in social behaviour and evolution. Following this, I went through my Master’s studying animal behaviour, in the context of evolutionary processes, and then I came to Florida to do my PhD. To this day, I have basically continued to develop my passion for the fantastic biology of termites, which I’d argue is misunderstood by most people. 

Frank: I think conventionally, people probably think of them as being pests, right? They’re conceived of as pests, but your paper really celebrates their social structures and the fascinating way that they organize themselves. Just before we go into the study, I wanted to ask, would you call termites your favourite organism? I’m sure you’re going to say yes…  

Thomas: Yeah, but I’m kind of biased. As I said, it’s what I’ve been doing all my working life.

Frank: Is there anything on the horizon? Any other organisms that you would love to study? Perhaps ants? 

Thomas: Everybody grew up as a kid seeing ants. We are exposed to ants, but rarely termites. They’re small and cryptic, and mostly restricted to tropical areas, so I was lucky to be exposed to termites early in my undergrad studies. I wanted to work on ants initially, just like everyone else; but the Burgundy University in Dijon, France, had some interesting live colonies of termite species from various parts of the world. It just blew my mind because I didn’t even know about the existence of such things. After a few days working in the lab as a volunteer, I knew that this was it and I wasn’t going anywhere. As an entomologist, overall, I do enjoy anything with 6 or 8 legs! I love to take my camera and snap anything that moves in the backyard. It’s very cool to look at the diversity of life out there, especially arthropods as a whole which represent the wonderfully wild levels of diversity in the world. Often, people don’t notice these things, and I view it as a pleasure to expose myself and my daughter to the outside world—something she seems rather receptive to!  

Frank: Children are sponges and blank canvases. We can impose really great traits on them just by exposure to as much as possible. So, being in Florida, I know you mentioned before we started recording that it’s a hotspot for invasive species. Can you dig into that a little bit and explain why that is? Following this, can you discuss this with specific focus on termites? 

Thomas: Florida is a unique place in the world (from the US perspective). We look at places like Australia which is a classic case of an island which has been invaded by lots of species that have destroyed ecosystems. We have a very similar case in Florida. We have major ports throughout the coastal areas of Florida, really large traffic of boats—commercial and private—which have gone around the world. Because we are in a tropical area, we are able to host species throughout the tropic range. The climactic conditions are favourable for these species to thrive. Over the past 100 years, we’ve had many invasive species introduced like snakes, reptiles, aquatic weeds, insects, etc. These have been introduced both with intent and by accident. Once they establish themselves, they wreak havoc in native ecosystems and agricultural areas. We’ve been hit really hard in the last few years with an insect that has caused massive damage to the citrus industry, for example. 

So, we understand very well in Florida the cost of invasive species which change the dynamic of ecosystems and economies. It’s the same for many social insects, like ants—we have more ant species than anywhere else in the country (maybe not Texas)—and more than 25% of these ants are invasive species. With termites, we have a similar situation. We have 20 species of termites, again more than anywhere else in the country, and about 5 or 6 which are invasive. A quarter of all species are invasive! These have come from boats coming in and out of ports, or sitting in marinas for years, and the next thing you know, a species comes to to be part of our regular landscape and we have to learn to live with them. Once they’re here, that’s it, we can’t get rid of them.  

Frank: That’s what I wanted to unpack. I know that sometimes the term ‘invasive’ can perhaps be a pejorative. Is there any evidence of invasive species benefitting the Florida ecosystem? Are there examples of any happy coexistences?  

Thomas: I agree that the term ‘invasive’ has anthropomorphic and negative connotations, because invaders for humans signifies something bad. It’s true that we look at ecosystems where species were introduced by human societies that have changed the ecosystems. The thing we must guard against is conceiving of ecosystems as having a natural state that cannot undergo any changes. People see it as bad because it’s “not like it used to be;” however, as an evolutionist, that’s what’s been happening for millions of years before we had anything to do with introducing invasive species to non-native locales. We are accelerating things, but it’s important to bear in mind that species coming into an ecosystem and changing the makeup can be viewed neutrally. Things change all the time, and sometimes we have something to do with it, and sometimes we do not. 

Frank: Let’s move on to the paper. Before I ask you about the paper itself, I was wondering if you could unpack some of the terms such as eusociality and biparental and alloparental care. 

Thomas: The joy of jargon in science… I’m glad you asked me this because we must make sure science is accessible for everybody. Eusociality is a term that basically describes groups of animals (not just insects, some mammals like mole rats do it) that live in a group where there’s a clear definition on who is performing which actions. So, you’ll have a reproductive division of labour which means very few individuals are doing all the reproduction in the colony while everyone else forgoes their ability to reproduce. We also have overlapping generations, which means that within the colony, we have many generations that succeed one another over a number of years. We also have a situation where some or most individuals (which aren’t the parents) are involved in taking care of the young (cooperative brood care). In social insects, this shifted so that parents largely just reproduce and the task of brood caring and other functions of the colony are taken care of by workers or ‘sterile castes’.  

Frank: Fantastic! This seems like quite an all or nothing strategy, To have a very small section of a population able to reproduce. What’s the evolutionary advantage of this kind of set-up? 

Thomas: Great question! This got me interested in the field of research I’m currently working in. Historically, most of the work has been done with ants and honeybees as models for understanding the evolution eusociality. Fantastic work has been done over the past 50 years to understand how these insects became so evolutionary successful. In plain terms, it’s a cost-benefit analysis from the insect’s perspective. There’s definitely a trade-off, and, depending on the selective pressure, it can be a winning or losing strategy. However, if you look at the entire animal biomass on earth, I think the latest estimation is that ants and termites represent more than 50% of animal biomass—just ants and termites alone! So I would argue that it’s a very well-winning strategy.  

The way they do it is that they decoupled the concept of reproduction and fitness. Here, some people like to use the idea of a superorganism in eusocial insects where we have a higher degree of complexity. As an individual, my cells represent different parts of my body that form organs with specific functions. For ant/termite colonies, this idea basically plays out at the colony, rather than individual, level. Some individuals focus on defense, digestion, reproduction, etc. The tasks have been split amongst individuals so that you look at the biological entity—not through the individual, but the colony as a whole.  

Frank: Fascinating. Let’s talk about the paper now. Could you explain the novelty of the paper and some key take-aways/results. 

Thomas: I was motivated to work on this by the fact that most of the theories on social evolution in insects has been done on ants and bees. Often, a lot of these concepts have been wedged into termite biology. I wanted to take a step back and go back to the fundamental differences in the biology of termites compared to other social Hymenoptera. They (termites) are diplo-diploid, monogamous (the king and the queen remain together for decades), and none of the individuals in the colony are predators—they feed on wood— while other social hymenoptera are reckoned to have reached eusociality via predation. So, again, the routes and conditions—in which the different systems have evolved eusociality as an evolutionary convergence—are very different. I wanted to know: what happened 150 million year ago to that cockroach ancestor that became the first termite? Some fantastic work has been done in the last few decades regarding how termites became termites, but I wanted to pinpoint the behavioural aspect which really changed everything for termites. In the paper, I wanted to show that in this proto-termite, as the mum and dad were stuck in a piece of wood (a poorly nutritious resource)—where the larvae take forever to grow and are stuck for years—protected in this environment where they live in their own food, the shift of parental care from the mum and dad began to happen. The eldest offspring would start to display these behavioural patterns of parental care which precipitated termites becoming social. Suddenly (from an evolutionary time scale), there’s more time for reproduction because some of the first cohorts of offspring started to take care of the next generations. 

The interesting part of my study is that if we look at the first few months of the ‘life’ of a colony, the male and the female are technically ‘wood roaches’. Mum and dad are taking care of everything: mating, laying eggs, caring for the eggs (via depositing salivary secretions to prevent desiccation of the eggs), feeding the larvae, and providing all the resources and nutrition to their growing young—they give everything they’ve got! They’re running on fumes within a few months because they’re dedicated to invest everything into the first generation. This jumpstarts the economic engine of a colony. As soon as the individuals, that are still technically larvae, become competent (able to chew on wood and digest it) they can start giving care to soldiers and the young, and feeding back to mum and dad. As this behaviour emerges in an incipient colony, we have this shift from biparental (mum and dad doing everything) to alloparental care (everybody else is doing the brood care). That shift is very obviously apparent as soon as the workers are ready. The very cool thing about termites, which differs from other social hymenoptera, is the fact that juvenile individuals (or, from one perspective, individuals stuck in a juvenile physiology forever), that do express adult behaviours of parental care. In termites, the shift of behaviour has emerged in juvenile individuals which allows the colony to become a eusocial group. Before this, it’s just a sub-social cockroach colony. Suddenly, we have cooperative brood, overlapping generations, and a reproductive division of labour.

Frank: That’s amazing! I think this is fascinating, so could you please further delineate some of the differences between ants and termites. 

Thomas: Well let’s say the big dogma was, and still is to some extent, inclusive fitness. In social hymenoptera, we have a haplodiploid system where societies are led by females—where the males only have half the genes and they only show up to mate and die. This means—at least as far aswe understand the emergence of eusociality in ants—75% gene similarity among individuals within the colony. In termites and most other eusocial systems, I’d argue we are dealing with a diplo-diploid system, where male and female have all the sets of genes and therefore all the brothers and sisters in the colony share about 50% of the genes. This is typical in a monogamous system—on average, all the offspring have about 50% of similar genetic similarity, half inherited from mum and half from Dad, which is random through the meiosis process.

We’re dealing with relatedness among individual termites which is lower than in other social hymenoptera, at least initially when eusociality emerged, so it was always hard to argue the inclusive fitness theory in termites. 0.5 is still pretty good, and it’s better than 0, I would argue. However, you still need to have a family unit where you share your genes, but the idea is that ‘if I help my brother and sister in the colony’, to help them grow into an adult and make a new colony, a big chunk of my genes will be passed on in the process. If you do the simple math for a colony of 1,000,000 termites (that can produce, say 50,000 alates, winged individuals, every year once the colony has reached maturity), from a worker perspective, one just needs seven or eight of these elates to successfully establish a colony in order to have 99% of my genes passed to the next generation. Now this again is a very anthropomorphic perspective; however, because termites rely on chaos and luck, they’re playing a numbers game. Instead of having one individual trying to succeed on its own, what they do is they all swarm at the same time. You have billions of alates swarming in the environment and most of them will be eaten. However, all it takes is just a few to survive to pass on genes to the next generation. From an evolutionary perspective, It works very well and there is very high success. In this case, ants and termites have so much in common through evolutionary convergences. 

Frank: Fascinating. Thank you for that explanation. Perhaps I’ve been watching too many dramas about people vying for thrones. I wanted to understand how ascension works. As you said, some will fly the next to seek their fortunes. How does it work within the colony if the two parents die? How does selection work for reproductive division of labour? 

Thomas: This is a very cool question. There’s a few things we know, but lots of things we don’t! A lot of work has been done, again, in ants. Allow me to backtrack, for every 1 termite biologist, you might have 25 ant biologists which explains why we’re quite behind. The idea is the king and queen termites are the longest-lived insect on earth. We think they’re able to live for 20-30 years, although it’s hard to tell. They’re very good at surviving for a very long time. If they die, depending on the species and the group of taxa that exists, some individuals can take over reproduction. Perhaps an individual that could’ve become a nymph and turned into an alate to fly out, will just stay and start mating with one of their parents, or with one of their brothers/sisters, I.e., inbreeding. However, it seems like the termites can tolerate inbreeding for some time quite well because it allows them to continue producing a massive amount of eggs, and most of them are sterile anyway so the long term evolutionary consequence of inbreeding is basically null. All it takes is a few of the next generation turning into an alate and mating with other individuals in the environment away from the colony to restore heterozygosity. 

Frank: Fantastic. I think we’ve talked about the germination of the idea, perhaps we’ll move on to the crystal ball section of this podcast! You’ve said that termite biology is behind ant biology, so, in your eyes, where should the research be directed towards next? What changes do you hope your work will precipitate and what do you want to see developing? 

Thomas: I consider myself as a behavioural ecologist to some extent, so I definitely want to go back to the shift of behaviour and see how it correlates with the activation of specific genes within the brains of individuals—especially in the king and queen, where it’s very hard to work with them because they are not found easily in the wild. To get around, we grow them by the thousands in the lab by collecting alates from the field and making young colonies. So we have the access to the kings and queens and we can start looking at their specific biology which has been mostly ignored. This has been ignored because we’ve largely focused on the workers and soldiers, which are relatively easily accessible in the field.

Furthermore we also want to look at the colony level, because in the past we’ve only been looking at the biology of the very few individuals that we collect in the field. These are taken out of the context of the colony and therefore out of the context of social complexities of life in a colony. We can now see everyone in small colonies in the lab—who’s doing what, when, and potentially why, which are always the most interesting questions. As I started looking at the king and queen, they do or don’t do things that are certainly surprising. I want to understand why they behave the way they do, and, ultimately, assess how their behaviour changes from the moment they start the colony to the moment they become the sole reproductives, with division of labour and are taken care of by their offspring. There’s a fundamental shift in the physiology, biology, and behaviours of termite kings and queens. I want to see how these correlate to improve our understanding of this transition, and we can then potentially identify candidate genes that are the causes of social behaviours. 

Frank: So, just before we wrap up, I was going to ask you if you wanted to do some shout outs? Perhaps a supervisor or teams you’ve worked with? Just before though, I’d like to go back and talk about some of the programs that you’re involved in. So you’re involved in the UF/IFAS School of Structural Fumigation, the Termite Course For Professionals, and the International Termite Course. Could you just let our listeners know what’s involved in these? 

Thomas: So, as a termite biologist, if I say to someone “hey, I work on termites,” they will usually ask me “how do I kill them?” I cannot just work on termites and not know how to kill them if they are chewing on your house. So I as I have an extension appointment here at UF, I where I need to cater for the public. I do it directly or indirectly through the pest control industry to make sure that the industry has the tools to help homeowners. So I dedicate some of my time to making sure that the industry is properly trained with the most current knowledge in science and within the regulatory framework for the use of pesticide. This varies a lot from country to country and even from state to state. The theme for the School of Structural Fumigation is a unique program where we bring people from around the world and we spend an entire week explaining how to perform a fumigation that is within the rules, is efficient, and is safe. For a quick run through, it’s a very dangerous product to use and the idea is that you inject the gas, to kill anything that is in the structure, including bed bugs, ants, rats, cockroaches, etc—basically anything that is impossible to locate in the building. You then remove the tent, the gas disperses, and you’ve basically then reseted everything. It’s illegal in a few places around the world, and where it’s legal, it’s heavily regulated. As a whole, it kind of opened my eyes about the reality of termites beyond their coolness and their evolutionary ecology.

However, I am able to indulge my love for termites because I organize, every other year, the International Termite Course for academics. During this course, we bring together termite biology graduate students, postdocs, and anybody who is interesting about termites and we spend a whole week just nerding out about how cool termites are. We share information, we start collaborations and our goal is to move termite science forward in a way that is more modern and more interactive. We want to achieve this with more collaborations from different teams around the world because we were still playing catch up in many ways compared to ant and bee researchers. 

Frank: So I think we’ve shone a quite positive light on termites so far. I just wanted to know, and this is coming from a layperson, everyone just thinks that they destroy structures and they’re terrible and they need to be killed. How do they assist or what are their functions in ecosystems? Is there anything like that? 

Thomas: That’s probably the most important question of the day. So there’s about 3000 termite species around in the world, mostly in the tropics, but also in some warm/temperate areas. Most of the species have a fundamental ecological function where they allow for the carbon cycle to exist. In some tropical areas, ecosystems without termites would collapse. They are some of the few species that can unlock the carbon stored in wood. They also participate in bioturbation, which means they move the nutritional aspect within the soil—they move things around in the soil—far more than earthworms, we argue, in many parts of the tropics. And out of this 3000 species, maybe 100 have the potential to be pests, so the vast majority of termites are doing their thing in environments and never run into with people. The problem is that we build things that are made out of wood and we grow things that are made out of cellulose—which includes agricultural commodities like tea and sugar cane—which some species feed on. So we have agricultural pests and then we have a handful of very bad structural pests and these five or six species are giving a bad rep’ for everybody. Basically, these are the ones that people care because they’re feeding on their houses. They a big economic impact around the world. I think the last estimate 10 years ago was about $40 billion in damages worldwide, every year. Therefore, in the psyche of societies, termites need to be eradicated. It’s a shame that most of the public probably thinks that there’s nothing good about termites. I understand where this comes from. It’s because there’s a reality that societies we live in. But I feel I’m one of the few lucky ones, with some of my colleagues and students, because we get to see how cool termites can be, most of them aren’t bad and nearly all of them are very important to the functions of ecosystems.

Frank: I’m sure someone much smarter than me can do some kind of Marxist analysis of termites attacking commodity and alloparental care representing some sort of socialist plot… But we’ll wrap up there. Before we do, Is there anyone you’d like to give a shout out to.

Thomas: Well, I am not here on my own and I didn’t come here on my own. I’m very lucky to have been mentored by a group of scientists in France—Christian Boudreaux and Alain Robert, who were my predecessors. They exposed me to how cool termites are, and then I came to Florida to do my PhD and I was able to work with Nan-Yao Su—my supervisor. Nan-Yao revolutionized how we deal with termites in structures in a way that reduces pesticides to a point where the industry has really changed for the better. I’d also like to shout out Rudi Scheffrahn, who has been very instrumental in putting the fume school together. Rudy has helped to make sure that it is a very successful program which ensures that fumigators are doing their work safely and efficiently. It was from Rudi that I inherited the program and it is my job to keep moving it forward. 

Frank: Well, thank you so much, Thomas. It’s  been a really lovely conversation. I’ve learned a lot and I’m sure our listeners will have too. Just to remind everyone, a transcript of this podcast will be available for anyone hard of hearing and links to the paper will be available, as well as the plain language summary for the paper. To finish, I just want to say thank you so much, Thomas.

Thomas: Thank you, Frank. It was a pleasure. 

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