Interview with a social insect scientist: Graham Thompson

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IS: Who are you and what do you do?

Who am I? For the past ten years, I have been a Professor of Biology at Western University in Canada. My research programme folds-in a lot of social insect research, to the extent that we have dubbed our lab ‘The Social Biology Group’. This is a fun moniker for us that I hope reflects our interest in the ideas that permeate the study of social breeding systems, rather than any one person (me) or taxon. My lab usually supports between 3-5 people – though currently, we are at ten – and for the non-human taxa in our lab, we like to mix it up! We keep honey bees, termites and even fruit flies as playthings and models to test cool, evolutionarily-minded ideas in sociobiology.

 

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Our lab logo – The Social Biology Group at Western University (Canada). For the Study of Behavioural Genetics and Sociobiology.

 

IS: How did you end up researching social insects?

I got lucky. In my final year of undergrad, I was inches away from graduating into the void of nothingness. I took a field course that the University of Guelph (Canada) offered at the time, in Jamaica. The course was a bit of a junket, I guess, but did expose many of us to tropical ecosystems for the first time. Most students frolicked in the foreshore of Discovery Bay, but I was one of the few students involved in a non-SCUBA project. I had freshly taken a course with IUSSI member Prof. Gard Otis and, having been intrigued by social insects in class, I found the arboreal Nasutitermes nests in Jamaica to be just the thing! Fatefully, on that same field course was my future MSc supervisor, Prof. Paul Hebert (who some may recognize for his later work on DNA barcoding). We ran some impromptu allozyme gels (it was the 90s) to decipher each termite colony’s breeding genotypes. I think I was literally the first undergraduate to actually use a Punnet square in real life, or so it seemed. It was amazing! Chance meets opportunity. I got into grad school. I’ve been living the dream ever since.

 

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Talking termites at the Biology and Genomics of Social Insects Meeting in Cold Spring Harbour, May 2018, featuring IUSSI members Mackenzie Lovegrove, Ed Vargo, Anna Chernyshova and, in the background, Guy Bloch.

 

IS: What is your favorite social insect and why?

I don’t really have one, or, at least, not a permanent one. But I can remember the glee of first finding Glyptotermes in rotten logs shortly after moving to Melbourne (Australia), as well as Coptotermes in giant mounds along the roadside near Canberra, Drepanotermes hoarding dried grass in their underground chambers in the Outback, and massive Neotermes in a suburban wind-blown Eucalypt. I also felt centred living along-side the mighty Mastotermes darwiniensis on campus at James Cook University in Queensland (where I once did a postdoc). This termite is a fascinating creature from another time, and sadly, is on its way out after a 200 M year reign. Maybe just a few million years left before its phylogenetic branch falls off completely? But these and other fleeting moments of biophilia do not tempt me to rank any taxon above another. Did I even mention bees yet? Plus, if I promote my favourite taxon at the expense of yours, as some do, inadvertently, with informercial-style talks at conferences, then I run a risk of coming across as a taxonomic chauvinist. I, therefore, think it’s best to keep our field taxonomically (and otherwise) diverse.

 

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Seek and you shall find: ‘Termite Avenue’ near Cairns Australia with fellow termite enthusiasts (L-R) Vernard Lewis, Becky Rosengaus, and Susan Jones. This photo was taken from an impromptu excursion from IUSSI 2014. A farmer had ‘planted’ termite mounds along his driveway as if they were hedges. #onlyinAustralia

 

IS: What is the best moment/discovery in your research so far? What made it so memorable?

As the late Ross Crozier once said, science is a grand tapestry of which we are all threads. Or something along these lines…anyway, when my Ph.D. supervisor was once asked this same question, he, being somewhat more poetic than me, conveyed to the interviewer that for him, discovery was as much about the people he was funding and teaching and training as it was about the biological discoveries they were making. Like Ross, I also view science as a social enterprise and my best memories are not necessarily centred around making single discoveries – although I am indeed proud of a few things – but rather the shared experience of doing so with others who have traveled, however briefly, alongside my science journey. I have met many such people along the way!

 

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A conference lost in time. With former Hamilton Award winner, the late Ross Crozier, who was my Ph.D. supervisor (1997-2000), and past IUSSI President Ben Oldroyd, with whom I did a postdoc (actually, two! 2003-2007) and who taught me everything I know about honey bees. Ross and Ben have been great mentors to me.

 

IS: If teaching is part of your work, what courses do you teach?  Has your work on social insects helped to shape your teaching?

I teach third- and fourth-year courses at Western University in Canada. Currently, Animal Behaviour and Behavioural Ecology, which are both right up my alley. I do let loose on the details of honey bee biology from time to time, to the delight of my undergrads. But I only do so as one of many possible vehicles to teach the ways and means of natural selection. I strongly prefer to explain biological concept over any specific content, and usually emphasize process over memorized particulars.

 

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One of our apiaries at Western University in action! With students (L-R) Kyrillos Faragalla and Anna Chernyshova. I am ‘supervising’.

 

IS: What is the last book you read? Would you recommend it? Why or why not?

I recently read The Price of Altruism by Oren Harman (Norton; 2010) and am meandering my way through two books by philosopher and biographer Ullica Segerstrale: Defenders of the Truth (Oxford; 2000) and Nature’s Oracle (Oxford; 2013). I met Ullica at a recent conference, and she deserves great credit for chronicling the on-going history of our field. All three of these books are biographical narratives of the people – George Price, Bill Hamilton, Ed Wilson, and others – whose lives, luck, insight, and in some cases, misfortune, shaped the academic turf on which we now play. I love this stuff.

 

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The Price of Altruism is high, as Oren Harman explains.

 

IS: Did any one book have a significant influence in shaping your career?  What was the book and how did it affect you?

At risk of sounding unoriginal, it was, of course, The Selfish Gene! I read it as a senior undergraduate and, in a whiff, the whole of my undergraduate training made sense, albeit, retroactively. It is bemusing to think that biology degrees are still taught by rolling out information piecemeal, course by course, without a grand unifying theme that ties it all together. The Selfish Gene did that for me, as it famously has for so many others.

 

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Lab photo 2017 (L-R) Anna Chernyshova, me, Anthony Gallo, Kristin Ransome, Christine Scharf, Julia Saraceni, Rahul Choorakkat, Kyrillos Faragalla and, missing from this photo, our three beekeepers:  Rick Huismann, Andrew Pitek, and Alex Guoth.

 

IS: Outside of science, what are your favorite activities, hobbies or sports?

Little known fact: I am an equestrian. I own my own horse and train with a coach to compete at shows. My horse and I are currently qualified for the Trillium Hunter Jumper Association Championships held in Toronto, the big end-of-season glitzy tourney for the top horse-rider pairs in the province (of Ontario). True story!

 

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Me and my trusty steed, a 16.3 hh Warmblood-cross gelding. On this day, he was Reserve Champion for his division.

 

IS: How do you keep going when things get tough?

I think the best quality for success in academia is sheer persistence. That, and playing the long game. Summer field season didn’t work out? -80C freezer went kaput? Paper sent to review for the third time? Funding pulled at the last minute? No problem! Dust yourself off and keep going as best you can. My advice, if you’re asking for it, is to stay consistent and persistent in your effort. We can all tolerate setbacks, even big ones, provided we recover quickly and keep going.

 

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One of our summer-long experiments in progress: feeding probiotic-infused pollen patties to increase performance and enhance resistance to disease. Or, we’ll see anyway!

 

IS: If you were to go live on an uninhabited island and could only bring three things, what would you bring? Why?

Sewall Wright’s Evolution and the Genetics of Populations Vols. I-III. We’ve all read Vol. IV, so no need to bring that.

IS: Who do you think has had the most significant influence on your science career?

A mentor who infused me with confidence and direction? An inspiring colleague who made academia fun when, without them, it wouldn’t have been? An influential author who taught me all I need to know? A friend who rounded out your life away from the lab? Your lab mate who killed it and lifted everyone around them? For me, it’s all of these, all the time.

 

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Recruiting kindergarten beekeepers at Wortley Public School in London, Ontario.

 

IS: What advice would you give to a young person hoping to be a social insect researcher in the future?

Start early.

 

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It’s never too soon to begin your career in social insect research! My kids helping me tend the bees.

 

The Food Search Box assay – where do we go from here?

A blog post highlighting the article by N. Tsvetkov, B. Madani, L. Krimus, S. E. MacDonald, and A. Zayed in Insectes Sociaux

By Armo Zayed

 

Assay for spatial learning and memory

Assay for spatial learning and memory.

 

As central place foragers, honey bees have an amazing ability to fly several kilometers away from their colony to forage and then beeline back to their home without getting lost. Honeybee foragers can perceive and communicate spatial information via the famous waggle dance. But how are these traits encoded in the honey bee genome?

When Nadia Tsvetkov joined my lab in 2012, she was keenly interested in studying the genetics of spatial learning and memory in bees. She spent several months training bees to fly through mazes. The maze experiments were fun but took too long, and our sample sizes were far fewer than the hundreds of bees needed to tease out the likely subtle genetic effects on learning and memory. What we needed was an assay that was as fast and as easy to standardize as the proboscis extension reflex assay – the workhorse of insect olfactory learning and memory studies. We tried some different approaches (one involved a very beautiful but unwieldy maze constructed out of Christmas balls) until colleague Dr. Suzanne MacDonald, a vertebrate biologist at York University’s Department of Psychology, suggested that we try the food search task paradigm. The paradigm is commonly used to study spatial learning and memory in primates and rodents. A common protocol entails hiding toys or food in boxes within a testing arena that animals are allowed to explore. Over time, the animals learn and can recall the location of boxes that contain rewards.

So we set out to try a similar assay on bees. For prototyping, we used some common and inexpensive items; we made the testing arena of clear Tupperware containers and we employed several artificial flowers made out of Q-tips. After a few pilot assays, we decided that a small arena containing four flowers was the best compromise between complexity and length of the experiment. Nadia worked out the testing protocol that involved placing bees into the arena where one of the artificial flowers had a sucrose reward. Once a bee found and fed from the rewarding flower, it was removed and tested again for a total of three training trials. Finally, the bee entered the arena where none of the flowers had a sugar reward. This time, the bee had to rely solely on its memory to find the focal flower. Our data analysis showed that bees subjected to this test exhibited two telltale signs of learning and memory: they improved their ability to find the rewarding flower during training, and they were able to recall the location of the rewarding flower after training. The Food Search Box (FSB) was born.

We carried out two more experiments to test the utility of the FSB for studying spatial learning and memory in bees. We first compared the performance of nurses (young honeybee workers that nurse the brood) and foragers (older workers that forage outside the colony) in the FSB paradigm. While both nurses and foragers did equally well in the training trials, foragers did substantially better than nurses in the memory test. So, is it age (young vs. old) or behavioral state (nurse vs. forager) that is influencing spatial memory in the FSB? To answer this question, we carried out another study on same-aged workers. We treated these workers with either cGMP, which causes precocious foraging, or cAMP, which does not alter behavioral state. The cGMP-treated bees performed similarly to foragers in the FSB, while cAMP and the control bees performed like nurses in the assay. Taken together, the results of these two experiments indicate that behavioural state (nurse vs. foragers) is primarily associated with differences in spatial memory in the FSB.

We are very excited by the results of the FSB; we were able to test bees quickly without much attrition. It is feasible to screen hundreds of bees within a short period, opening up the door for genetic and genomic studies of spatial learning and memory in honeybees. While it is certainly possible to improve on the design to enhance automation (i.e., RFID readers or tactile sensors to passively record visits to artificial flowers), the low-tech version presented in the paper is very easy to set up and perform. We are looking forward to feedback from the community on the test, and we hope it will provide a useful tool for studying spatial learning and memory in honeybees and other insects.

Ants colonise bird nests and raise broods in them

A blog post highlighting the article by M. Maziarz, R. K. Broughton, G. Hebda, and T. Wesołowski in Insectes Sociaux

By Marta Maziarz

As an ornithologist, I have focused on the reproduction of birds but often overlooked the fact that bird nests can also be home to many invertebrates that find shelter, food or a suitable microclimate within them. When we discovered ant workers and their larvae inside nests of the wood warbler Phylloscopus sibilatrix, curiosity drove us to study this phenomenon.

An initial literature review revealed just a handful of published records of ant broods found inside bird nests, including blue tits Cyanistes caeruleus breeding in nest-boxes in Corsica (Lambrechts et al. 2008), and great tits Parus major and marsh tits Poecile palustris occupying tree cavities in primeval stands of the Białowieża Forest, Poland (Mitrus et al. 2015). Blem and Blem (1994) reported ant colonies on the side of nests in nest-boxes used by prothonotary warblers Protonotaria citre but gave no further details. This surprising scarcity of observations of ants in songbird nests suggested that this phenomenon may be exceptional and occur only among cavity-nesting species.

Our discovery of ant workers and their larvae in wood warbler nests, which are domed structures composed of dry grass, moss, and leaves and situated on the forest floor, challenged this view. We made the original finding during long-term studies of wood warbler ecology in 2004-2015 in Białowieża Forest (Eastern Poland), which prompted us to document this phenomenon systematically during 2016-2017. In 2017, we also contacted researchers in Switzerland and the UK to ask them to inspect nests for the presence of ants and their broods. We wanted to find the frequency of ants colonising wood warbler nests, and whether ants are present in wood warbler nests elsewhere in the species’ breeding range.

During our systematic observations in 2016-2017, we found adult ants in 43% of warbler nests, and one-third of nests also contained ant larvae or pupae. These ant broods were situated within the sidewalls of the nests, at or just above ground level. The most frequent species were Myrmica ruginodisor M. rubra, and occasionally Lasius niger, L. platythoraxor L. brunneus. These numbers, compared to 30% of nests containing adult ants and 20% containing broods during the earlier (2004-2015) period, indicated a long-term association between the ants and the birds. The findings from Białowieża Forest contrasted with those from Switzerland and the UK, where we only found single cases of adult ants and their broods. The different frequencies of ant presence between regions could be due to varying densities of bird or ant nests between woodlands transformed by humans to a different degree, but further studies would be necessary to confirm this.

These first records of adult ants and their broods in wood warbler nests showed that occupation of bird nests by ants can be a locally common phenomenon, which may have been overlooked previously in this and other songbirds. Systematic examination of nests belonging to different bird species would be valuable in understanding this further.

Furthermore, the occurrence of ant broods in the walls of wood warbler nests showed that ants colonised these structures following their construction by birds. Why they do this remains unclear; are the ants attracted to the nests by their structure, the presence of other invertebrates as a source of protein, or by heat generated by the birds? More work is underway to answer these questions, but it seems that these potential ant-bird interactions could be much more widespread than has been suspected.

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Wood warbler nests are dome-shaped and constructed of leaves, grass, and moss. They are usually hidden among low herb vegetation, under a tussock of grass or sedge, or wedged under fallen branches or logs. Such structure and locations could promote their occupation by ants, for example, Myrmicaspp., which raise their broods in similar places.

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Numerous ant Myrmicaspp. larvae and two larger, well-grown blowfly Protocalliphoraspp. larvae (centre-right) in the wall material of a wood warbler nest

References

Blem CR, Blem LB (1994) Composition and microclimate of Prothonotary warbler nests. Auk 111:197–200.

Lambrechts MM, Schatz B, Bourgault P (2008) Interactions between ants and breeding Paridae in two distinct Corsican oak habitats. Folia Zool 57:264–268.

Mitrus S, Hebda G, Wesołowski T (2015) Cohabitation of tree holes by ants and breeding birds in a temperate deciduous forest. Scand J For Res 31:135–139.

Microbiomes and worker tasks

Highlighting the article written by J. C. Jones et al. in Insectes Sociaux

Written by Insectes Sociaux Editor-in-Chief, Michael Breed

Molecular techniques for identifying microbial community composition have created a
true biological revolution. Recent discoveries lead us to understand the bacteria as an
evolutionarily complex and diverse domain, and this in turn has sparked interest in
characterizing microbiota from a large number of contexts. Of particular significance has been the exploration of gut microbiomes, which vary dramatically among species, and developmentally within species. Gut microbiomes interact strongly with diet and health, giving added interest to studies focusing on this subset of communities (Dunn 2011, DeSalle and Perkins 2016).

We have long understood the importance of the gut microbiome in social insect species. In termites, some components of the microbiota reduce cellulose to usable sugars while in other species, members of the microbiota fix nitrogen. More recent studies of ant and bee gut microbiomes have shown some level of intraspecific consistency even over broad geographic ranges, but also variation associated with diet and to a certain extent differences among colonies.

In this issue of Insectes Sociaux, Jones and her colleagues (Jones et al 2018) focus on
differences in the gut microbiota based on task group in honeybee (Apis mellifera) colonies. This is a question previously addressed by Kapheim et al (2015) but Jones and colleagues add critical dimensions by age-matching the worker bees in their study and collecting gut samples from bees observed performing specific tasks.

Each of five experimental colonies consisted of 1500 workers of the same age and from
the same source colony (400 of which Jones and colleagues individually marked). They
observed worker behavior in ten to fourteen-day old bees. Nurses, food receivers/handlers and foragers were noted and collected. This approach allowed assessment of diet and task-related differences in microbiomes independent of age-related developmental effects.

Jones et al (2018) found that Firm-4 (Lactobacillus mellis), one of the characteristic
bacteria of the honeybee microbiome, was more prevalent in nurse and food handling bees than in foragers. This pattern was also seen with quite a few other bacteria species, which had higher presences in nurses and/or food handlers than in foragers. One species, Lactobacillus kunkeei, was more common in forager guts, although they found it less commonly there, so this result is more provisional. Of particular note in the guts of food processing bees was Bartonella apis, as this species expresses genes that may be involved in the degradation of secondary plant metabolites.

Globally, the microbiomes of nurses and food handlers were more diverse than the
microbiome of foragers. Jones et al (2018) suggest that the needs for carbohydrate metabolism are higher for nurses and food handlers and that perhaps this drives functional differences in the gut microbiome between these task groups and foragers.

Concerns over bee health, responses of bees to diseases or parasites, and the impact on bees of the agricultural use of antimicrobials have generated much of attention given to bee microbiomes (Napflin and Schmid-Hempel 2018, Raymann and Moran 2018). While these topics are important, the microbiomes of social insects existed long before humans started to impact social species, and social insect microbiomes must have evolved alongside sociality. How might gut microbiomes facilitate worker task performance? Do they determine workers’ roles within colonies? The cause and effect relationship between task group and microbiome could go in either direction, with task environment driving the microbiota or the nature of the microbiological community feeding back into the task choice of bees. This study presents these alternatives as tantalizing avenues to pursue in future research.

References

DeSalle R, Perkins SL (2016) Welcome to the microbiome: Getting to know the trillions of bacteria and other microbes in, on, and around you. Yale University Press 264pp.

Dunn R (2011) The wild life of our bodies: Predators, parasites, and partners that shape who we are today. Harper 304pp

Jones JC, Fruciano C, Marchant J, Hildebrand F, Forslund S, Bork P, Engel P, Hughes WOH (2018) The gut microbiome is associated with behavioural task in honey bees. Insect Soc https://doi.org/10.1007/s00040-018-0624-9

Kapheim, KM, Rao VD, Yeoman CJ, Wilson BA, White BA, Goldenfeld N, Robinson GE (2015) Caste-specific differences in hindgut microbial communities of honey bees (Apis mellifera). PLoS ONE 10: e0123911

Napflin K, Schmid-Hempel P (2018) Host effects on microbiota community assembly. J Anim Ecol 87: 331-340

Raymann K, Moran NA (2018) The role of the gut microbiome in health and disease of adult honey bee workers. Current Opinion in Insect Science 26: 97-104

Does size matter when using celestial cues to navigate towards home?

A blog post highlighting the article by R. Palavalli-Nettimi and A. Narendra in Insectes Sociaux

By Ravindra Palavalli-Nettimi and Ajay Narendra

Imagine finding a location in a new city without any map. How would you navigate toward your destination?

If you were an ant, you could use celestial cues such as the position of the sun or the polarised skylight pattern (Wehner and Strasser 1985; Zeil et al. 2014) as a compass to navigate in the direction of your destination (e.g., nest). The compound eye of an ant has a few special ommatidia that are sensitive to polarised skylight (light waves oscillating in one orientation). However, the eye size and also the total number of ommatidia in the ants’ eyes decrease with their body size. Some ants have close to 4,100 ommatidia (Gigantiops destructor) in their eyes while a miniature ant has a mere 20 ommatidia (Pheidole sp.). However, it is not clear how this variation affects their ability to navigate.

 

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Size variation in ant heads.

 

In this study, we investigated how size variation affects ants’ ability to use celestial cues to navigate towards their nest.

To test this, we captured ants on their way to their nest and displaced them to a circular platform. The displacement site was at least 500-1,000 m from the ants’ nest and was surrounded by a creek. Thus, the ants had never foraged there and could not use landmark cues to navigate, but instead, they had to rely on celestial compass cues to walk towards their nest. We filmed the paths taken by the ants using a video camera and later digitized their head position frame by frame.

We found that having fewer ommatidia does not affect the ants’ ability to use celestial cues. The ants’ heading direction on the platform did not significantly differ from the fictive next direction. Since larger ants have greater strides and thus travel more distance for the same number of strides, we also analyzed their heading direction at a distance on the platform scaled to the body size of the ants.

We also found that the smaller ants were slower and had less-straight paths than the larger ants, even after controlling for differences in leg size (correlated with body size and head width) and stride length. This finding means that a reduced ability of the smaller ants to access celestial compass information results in a less straight path and reduced walking speed. However, the overall ability to initially orient towards the nest using a celestial compass is retained in miniature ants. Thus, while miniaturization in ants can affect their behavioral precision, it may not always lead to a loss of vital behavioral capability such as using celestial cues to navigate.

 

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Paths and heading directions of various ants that differed in head width and ommatidia count.

 

In conclusion, finding a destination in a new city might be a lot easier if we were ants—of any size—and could use celestial cues!

References

Wehner R, Strasser S (1985) The POL area of the honey bee’s eye: behavioural evidence. Physiol Entomol10:337–349.

Zeil J, Ribi WA, Narendra A (2014) Polarisation vision in ants, bees, and wasps. In: G Horváth (ed) Polarized light and polarization vision in animal sciences, Springer, Heidelberg, pp 41–60.