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.

 

Interview with a social insect scientist: Rachael Bonoan

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IS: Who are you and what do you do?

I am Rachael, a post-doctoral researcher at Tufts University (Medford, MA) and Washington State University (Vancouver, WA). As a post-doc, my focus is the natural history of an ant-caterpillar relationship in the South Puget Sound, WA. When it’s a caterpillar, the at-risk Puget blue butterfly is protected from predators by ants. For the next couple years, it’s my job to figure out which ants are in the community where Puget blue caterpillars reside, which ants tend the caterpillars, and how the ants behave while defending their charge. Once the caterpillar has been protected, it secretes a sugary snack as a “thank you” to the ant (or ants). (see photo below)

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Before starting my post-doc, I studied honey bee nutrition and behaviour in the Starks Lab at Tufts University. The main takeaway from my PhD: diet diversity is important for honey bees (and other insect pollinators).

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IS: How did you develop an interest in your research?

As far as insects go, I have always loved them. As a kid, I spent summer nights outside with my dad catching caterpillars, ladybugs, June bugs, whatever I could find.

How I got into social insects is a slightly longer story. As an undergraduate, I studied cognition in social birds. One summer, I was accepted into the Tufts University NSF Research Experience for Undergraduates (REU) Program where I did fieldwork studying butterflies. During the REU Program, I fell in love with fieldwork, but I missed the aspect of sociality. For graduate school, I decided to combine my two interests and applied to labs that studied social insects in the field. I ended up joining the Starks Lab to study honey bees and in studying honey bees, became enthralled with the world of beekeeping.

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IS: What is your favourite social insect and why?

This question is so hard. As a beekeeper and someone who recently got their PhD studying honey bees, I feel like I should say honey bees. I do love honey bees, but my favourite social insect might be leafcutter ants. The first time I went to Costa Rica and saw them in action, it was mesmerizing. They walk the same trails so often that they wear down a path in the rainforest. Ants wear down a path in the rainforest. Also, when it rains (which happens often in the rainforest), they just drop their leaf and run home. When the storm passes, they get right back to work!

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

One of my overall favourite studies was the subject of my very first graduate school publication. I worked with an undergraduate to study how worker honey bees cool the hive following heat stress. We heated a small section of a honey bee hive with a theatre lamp (very technical equipment), and took thermal images of the hive as it cooled down. We found that honey bees somehow radiate the heat out to the edge of the hive and in this way, cool the hive down in less than 10 minutes. The heated section of our control hive, the one without bees, remained hot even after 20 minutes!

This was also the easiest and quickest publication process I have ever been through. I submitted the manuscript in February, we quickly received positive reviews, and the paper was published by the end of April. My advisor told me to never expect an experience like that again.

P7From Bonoan et al. 2014: Comparison of representative experimental and control infrared images taken pre- and post-heating. The colour green indicates the presences of bees in the experimental hive and the heating pads in the control hive. Red and white areas indicate temperatures above 37 °C. In the experimental hive, the red area grew significantly larger within 3 min of cooling and disappeared within 9 min. In contrast, the high heat area in the control hive gradually decreased in size and still persisted after 18 min of cooling. Such differences indicate that workers effectively cooled the hive by absorbing the heat moving it into the periphery

Full citation: Bonoan RE, Goldman RR, Wong PY, Starks PT (2014) Vasculature of the hive: heat dissipation in the honey bee (Apis mellifera) hive. Naturwissenschaften 101, 459-465.

IS: Do you teach or do outreach/science communication? How do you incorporate your research into these areas?

Yes! Teaching, mentoring, and communicating are three passions I discovered while in graduate school. At Tufts University, I teach an undergraduate-level class called “From Bees to Beetles: Insect Pollinators and Real-World Science.” Students get assigned an insect pollinator that they follow throughout the semester and end the semester by creating a pollinator protection plan for their insect. The students read primary literature that we discuss in class, some of which are my own publications.

I also lead a program, “All About Bees,” at the Discovery Museums in Acton, MA. One of my favourite activities in this program is honey tasting. Before they taste various honeys side-by-side, many people don’t realize how different the honeys are! This gives me a chance to talk about how different flowers have different nectar chemistry, and different nutritional values for pollinators. I also bring microscopes for people to get an up-close look at tiny bee parts and when possible, I bring my teaching hive of live (but contained) honey bees.

I’ve also given various presentations about my honey bee research and the importance of insect pollinators in general to beekeeping associations, public school teachers, girl scout troops, high school students, etc.

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photo credit: Evan Sayles

IS: What do you think are some of the important current questions in social insect research and what’s important for future research?

The big important question that remains, and may always remain, is: how did sociality evolve? Insects provide a great study system for this question, especially when families or subfamilies of insects exhibit different levels of sociality, and the comparative method can be used. Apidae, for example has social bumble bees, gregarious carpenter bees, and thousands of solitary ground-nesting bees. Relative to social bees, there is very little research on solitary bees—maybe solitary bees hold an answer to evolution of sociality.

Investigating the evolution of sociality has also gotten bit more complex—and interesting! —with the development of tools to study the gut microbiome. This is highlighted in a recent Insectes Sociaux article by Jones et al. showing that the honey bee gut microbiome is associated with behaviour. Such findings could have implications in the development of the caste system and the division of labour. Thus, a more current question may be: how have microbes influenced the evolution of sociality?

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

The last non-fiction book I read was Journey to the Ants by Bert Hölldobler and E.O. Wilson. I would recommend it to anyone interested in social insects, ants, or science in general. The book does a great job covering the awesome things about ants while describing Hölldobler and Wilson’s beginnings in science.

The last fiction book I read was Caroline: Little House, Revisited by Sarah Miller. I would recommend this fanfiction book to anyone who loves Little House on the Prairie, like myself. The book tells the story of the family’s journey from the big woods to the prairie from Caroline’s (the mother, for any non-little house fans) point of view. I enjoyed seeing the journey from the mother’s point of view, and I found the author was true to the personalities and family dynamic of the original books.

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

I go few places without my camera. I especially enjoy getting down on the ground for some macro-photography.

I also love to read, bake, and whenever possible, get outside. I love hiking—my husband and I have a lifelong goal of getting to as many national parks as possible. So far, we’ve been to four together (I’ve been to a fifth without him).

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

Science, like life, never goes as smoothly as you want it to. That’s just how it is. It doesn’t mean you’re a bad scientist, or you’re a failure, or you don’t belong. When things get tough, I try to remind myself of this. Science is a challenge and a continuous learning process, which is why I love it. It’s also helpful to talk through things when I feel a bit down in the dumps about an experiment, or something goes awry in the field.

When I start to feel overwhelmed by trying to do too many things in general (which I sometimes do), just being outside is my remedy. Driving out of the city to a place where I can breathe in the fresh air, and smell pine trees, usually resets me.

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

Oh man, this is tough. If I can bring a person as my “thing,” I’d bring my husband. I’d also bring my Swiss Army knife and my Red Sox hat, both of which I rarely do fieldwork without. Both are useful, but also have sentimental value and would remind me of home.

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

Over the years, I have had so many amazing mentors, it’s hard to pick one.

My very first mentor in science was my high school biology teacher, Mr. Saunders. In Mr. Saunders’s class, we did an experiment that required watching a goldfish open and close its gills, so we could measure respiration. It may sound tedious to some, but I loved it! That was the moment I realized I wanted to pursue science.

Also, Natasha, my REU mentor during my first field experience was huge. Natasha showed me that it was possible to do science outside! It was that summer that I realized I could have a job outdoors, observing and/or chasing insects.

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

Stay curious. As we grow up, our natural curiosity that is at the forefront as children, tends to get pushed toward the back. Holding on to that childlike curiosity will help you be a better scientist and a better citizen, no matter what you study or where you call home.P5

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.

Interview with a social insect scientist: Luke Holman

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IS: Who are you and what do you do?

Hi! I’m a Senior Lecturer working at the University of Melbourne. I did my undergrad and PhD in Sheffield, UK. My PhD was on sperm morphology in fruit flies, and I began working on social insects during my first postdoc at the University of Copenhagen with Prof. Patrizia d’Ettorre. Since discovering a bunch of ant, bee, and wasp queen pheromones in 2010-14, a lot of my research has focused on working out how queen pheromones evolve, how they work, and what they can tell us about the origins of eusociality. Currently, I also work a lot on sexual selection and ‘meta-science’ (including topics like p-hacking, research methods, and the gender gap in the science workforce), and I teach undergraduate genetics and evolution.

IS: How did you develop an interest in your research?

In short, I read most of The Selfish Gene during high school, and realised evolutionary biology was incredible! It was earthshattering to realise that we could make sense of nature’s astounding complexity and weirdness using simple, logical theory. Initially my research focused on puzzling traits that seem to defy conventional evolutionary logic: my PhD was on a group of flies that produce thousands of specialised, infertile sperm (apparently on purpose). Are these sterile sperm a worker caste that help the fertile sperm somehow? Or are they casualties of intragenomic conflict? We still don’t really know, but I was hooked.

IS: What is your favourite social insect and why?

Probably the black garden ant, Lasius niger, for changing my life by making my career in science possible. If it weren’t for their reliably massive mating flights in the parking lot outside my office in Copenhagen, I would not have had such a successful first postdoc. Each year I could collect up to 900 queens in a couple of hours, enough for a whole summer of experiments, simply by strolling around on summer evenings. A close second is the ant Lasius flavus, because they’re bright orange, very gentle, and have a nice simple cuticular hydrocarbon profile that’s easy to analyse by GC-MS.

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

Probably the day I isolated the queen pheromone of Lasius niger. I moved to Denmark in summer 2008, and on Patrizia’s advice I began my first experiment with synthetic pheromones, on boxes of ants kept in my living room (they needed to be treated twice daily with pheromones for a month). At the same time I was working day and night on a Marie Curie fellowship application, and exploring the new city. I ran the whole experiment blind, so for ~2 months I had no idea if the putative pheromones were doing anything. After collecting all the blind-coded data and making the graphs and statistics, I took them to Patrizia’s office for decoding, and we realised that we had isolated arguably the first ant queen pheromone. That felt great! As well as being a significant discovery, it was a lucky break that set the stage for a productive postdoc.

IS: Do you teach or do outreach/science communication? How do you incorporate your research into these areas?

I have written a little for The Conversation, which is a great website – for those that don’t know it, it hosts science journalism explained in plain English by actual researchers. I’d encourage your readers to contribute to it: it’s a non-profit enterprise with a large readership that provides a good antidote to mainstream science journalism, which is hit-and-miss. In my lecturing, I certainly touch on my own research interests, but I have also been surprised by how much my teaching has helped my science. Many times, I have been writing lectures and realised that I didn’t properly understand something, or I have noticed papers or knowledge gaps that lead me to a new research project (particularly when I have been asked to teach something outside my comfort zone).

IS: What do you think are some of the important current questions in social insect research and what’s important for future research?

The question that springs to mind is “Does methylation matter?” There are many review papers arguing that social insects use DNA methylation to regulate caste polyphenism, but precious little data, and most of the data that we do have is non-experimental and uninformative (e.g. “We looked at the methylome of one queen and one worker, and found some differences”). There’s a widely-cited 2008 Science paper showing that experimental manipulation of DNA methylation causes larvae to develop into queens, and we could settle the question by replicating or expanding this approach.

More broadly, I think social insect research would benefit by incorporating recommendations from the ongoing “Reproducible Research” movement: open data, good experimental design, transparent statistical analysis, etc. In a recent meta-analysis, I showed that 70% of queen pheromone experiments were not conducted blind, and that non-blind experiments had hugely inflated effect sizes (presumably due to observer bias). Sample sizes were very often strikingly small (e.g. n=6, barely enough to analyse), making these studies almost entirely uninformative. Given that social insects are known for being numerous, I don’t think it’s unreasonable to insist on large, blind, well-designed experiments. I have also found that many flat-out social insect scientists refuse to share or archive their raw data, hindering research synthesis and ensuring that their results are unavailable for re-use or fact checking.

IS: What research questions generate the biggest debate in social insect research at the moment?

Unfortunately, the answer is probably still the continuing fallout over the 2010 Nature paper by Nowak, Tarnita and Wilson! For my part, I am baffled by both sides. The original paper made various obviously untenable claims, e.g. that kin selection theory has made only a “meagre” contribution. However I also find it odd how much effort has been invested in rebutting this paper: there are dozens of papers replying to it, and I have sat through multiple angry conference talks. At some point I think we just need to shrug and get on with it. An uncomfortable truth is that all science is somewhat wrong, and I’m not convinced that doing science “at” a particular person/group is a useful way to advance knowledge.

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

I Contain Multitudes by Ed Yong, about the microbiome. Absolutely fascinating read with Ed’s characteristically playful, funny style. A sample factoid: some researchers think that humans and bacteriophages have co-evolved. Our gut is lined with mucus that just so happens to be a great habitat for phages to lurk and take out bacteria that try to get through the gut lining. I never thought that I was involved in a mutualism with a virus!

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

I like travel, hiking, rock climbing, yoga, and meditation. In the past I was cripplingly addicted to juggling, and spent many hours a day throwing small sacks of seeds in the air; my record was 8 balls for about a second, or 5 balls for about a minute. I also spend plenty of time reading the news and fretting, though I’m trying to cut down.

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

The last 2-3 years have been very stressful, as I made the transition from postdoc to lecturer. Instead of doing less science to make room for my new responsibilities, I just worked harder, which was a bad idea as I ended up burning out. I now try to leave work on time and keep active, but years on fixed-term contracts has left me with a loud inner voice that shouts, “You should be publishing!”. I’ve been lucky to have lots of supportive friends and family to lean on, but I think the best way to manage in tough times is to make sure you’re not already exhausted by your normal work. Maybe the answer is to sit down and plan for your mental health and well-being, just as you would plan for a field season.

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

Swiss army knife, water purifier, and a boat to get off the island.

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

Probably WD Hamilton. Reading his 1964 papers, it’s amazing how many future branches of evolutionary ecology he foreshadows in throwaway sentences. Also, I likely wouldn’t have become a scientist if his work wasn’t evangelised so well in The Selfish Gene. As for people I’ve actually met, I pick my second postdoc advisor, Prof. Hanna Kokko. I try to emulate her incisive way of thinking, her efficient work practices, her skill in balancing work and life, and her kindly enthusiasm for everything.

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

I’d recommend keeping up with research outside as well as inside the social insect world! To its detriment, a lot of social insect research is focused on narrow, taxon-specific issues, and only uses methods that have previously been applied to social insects. This slows down the pace of development in social insect science, and reduces its appeal to researchers from other fields. Some of my best papers involve applying a widely-used concept or method to social insects in a novel way. For example, dozens of non-social insect people work on ‘intralocus sexual conflict’, the concept that there is antagonistic pleiotropy for male and female fitness, leading to maladaptation in both sexes. I pointed out that the same thing applies to queens and workers: basically, it’s hard to make a perfect worker and a perfect queen using the same genome, so each caste ends up a little bit maladapted. Another example involves the analysis of gene expression data. Most social insect transcriptomics studies test each gene for differential expression one at a time, but in other fields it has long been commonplace to also test for differential expression in ‘modules’ of strongly co-expressed genes.

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.

Welcome to the new Insectes Sociaux social media team

Hello social insect fans,

It is my pleasure to introduce the new social media editing duo for Insectes Sociaux, Bernadette Wittwer and Madison Sankovitz, coming to you from Australia and the United States respectively. Having worked with them over the last month to hand over the reins to the Insectes Sociaux social media accounts, I can tell you that they have lots of exciting things planned for you, including an Instagram account (@insectessociaux)!

Madison Sankoviz

I am an entomology Ph.D. student in the Purcell Lab at the University of California Riverside. My research interests are the ecological interactions and biogeography of ants. With a passion for insects and understanding the dynamics of changing ecosystems, I am interested in answering questions of what social and behavioral traits allow survival in the extremes of latitudinal and elevational gradients in Formica ants. I also explore ant-mediated soil manipulation. Passionate about teaching and communicating science to the public, I am the graduate student coordinator for our department’s outreach program. I received a B.A. in ecology and evolutionary biology from University of Colorado Boulder, where I studied the effects of Formica podzolica ant colonies on soil moisture, nitrogen, and plant communities. Not only am I constantly inspired by the research of other social insect scientists, but I admire their enthusiasm for the natural world. I look forward to highlighting future publications and investigating the stories behind them as a social media editor for Insectes Sociaux!

Bernadette Wittwer

I am an evolutionary biologist with research interests in broad evolutionary transitions. I competed undergrad and honours at the University of Queensland. My honours research examined the evolution of feeding behaviour in crocodilians, with a focus on Isisfordia duncani, a 90-million-year old crocodile from western Queensland, Australia. After honours I moved to the University of Melbourne and undertook my Ph.D. looking at the evolution of communication in bees. Bees have an extraordinary depth of behavioural diversity and it is through them that I was introduced to the wonderful complexities of insects that live in groups. My research has particularly focussed on antennal structures and how bee species have adjusted their investment in communication as they have evolved different social behaviours. Through my research I’ve been grateful to work with and meet so many enthusiastic social insect researchers and I look forward to exposing more wonderful social insect research through Insectes Sociaux’s social media channels.

The best part of this role has been working with all the contributors to the blog and our interviewees. Thank you again to all of you that have participated.

If you are interested in blogging or interviewing, do not hesitate to contact Bernie and Madison via Twitter (@InsSociaux), Facebook, or via email at bernie.inssoc@gmail.com and madisoninsectessociaux@gmail.com.

Interview with a social insect scientist: Roberto Keller

RobertoKeller-2016-04-Lisboa

IS: Who are you and what do you do?

RK: My name is Roberto Keller. I grew up in Mexico City where I majored in Biology, later pursuing a PhD in Entomology up north in the USA, and since the past decade I live in Lisbon, Portugal, currently working at the Nacional Museum of Natural History. I’m a comparative anatomist that specializes in ants.

IS: How did you end up researching social insects?

RK: Back at the University in Mexico the people in our group of insect enthusiasts was choosing which taxon to specialize on. Most of my peers were drawn to shiny scarab beetles, some into colourful butterflies, but I loathed those clichés so I placed my attention into all those little brownish ants running around. Once I looked at them under the stereoscope I was surprised at how elegant and varied ants can be. I was instantly hooked. Oh, that and the fact that I never liked to mount insects with wings because getting them to look right is just a pain.

IS: What is your favourite social insect and why?

RK: Neoponera apicalis. This is an ant species that lives in the tropical forests from Mexico to South America. The workers are large, matte black, with the tip of their antennae light yellow. Workers forage alone on the shaded damp forest floor, so you only see a pair of yellow antennal tips dancing around. The first time I saw one I was so excited that I grabbed with my bare hand. Their sting feels like a painful electroshock.

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

RK: I was once reading a short paper comparing the external morphology of queens versus workers in an ant species. The whole discussion was off because the authors had wrongly assumed that the largest thoracic segment in workers was the fusion of the first and second segments when compared to queens. My first reaction was to rail against the authors for making what I consider an obvious mistake. It later hit me that not only was their error quite understandable, but that it pointed to a remarkable difference between those two castes that had been in front of me for years but I had been blind about until that moment.

That turned into a productive research project and taught me to keep a keen eye and question the obvious. I learned a lot from that short paper even with its errors, and I think that this is how science keeps moving forward— we built upon the work of others and hope that the next person who comes will be able to solve the things we were too short sighted to see.

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

RK: I teach courses in general Entomology and, once in a while, on ant morphology. I can’t think of a way in which studying social insects has influence my teaching. I often forget that ants are social, it’s bad. That is why I have collaborators: to remind me.

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

RK: I’m finishing Steven Pinker’s latest book Enlightenment Now: The Case for Reason, Science, Humanism, and Progress. It is appalling to me seeing that we live in a very modern society, and yet we have political extremes converging on pure irrationally. This is a good book to remind people how much science has benefit humankind as a whole, but I’m afraid the people who will read it already know this.

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

RK: Once I was hooked learning about ants during college I got myself a copy of Hölldobler and Wilson’s The Ants, which had been recently published. The dedication reads “For the next generation of myrmecologists.” I felt they were talking directly to me and that dispelled any doubts I still had about following a career in social insects. So at the end I am that cliché I was trying to avoid.

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

RK: I’m a portrait photographer. I’m intrigued about people, and portraiture allows me to sit down for a brief face to face conversation and try to capture that interaction through an image.

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

RK: I like to follow the advice of philosopher Paul Feyerabend:

“If you want to achieve something, if you want to write a book, paint a picture, be sure that the center of your existence is somewhere else and that it’s solidly grounded; only then will you be able to keep your cool and laugh at the attacks that are bound to come.”

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

RK: Hmm, can’t think of any objects that will make sense with the prospect of solitude other than hemlock.

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

RK: My parents. Both chemists, they created a growing environment for my siblings and me in which science was a natural part of life.

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

RK: Don’t grab large social insects with your bare hands. Unless they are termites. Termites are always safe to grab.

 

Interview with a social insect scientist: Hollis Woodard

thumb_UCR S. Hollis Woodard 2016 64 copy_1024IS: Who are you and what do you do?

HW: My name is Hollis Woodard and I’m a bumble bee biologist and an Assistant Professor in the Department of Entomology at UC Riverside. My lab group works on all sorts of things to do with bumble bees, including their nutritional biology, social organization, foraging ecology, and more.

IS: How did you end up researching social insects?

HW: I fell in love with social insects during college when I took an evolutionary biology class. We had a lecture on sociobiology and talked about insect societies and division of labor and I remember thinking it was the most interesting thing I’d ever thought about. I already had an incipient interest in social behaviour because I’d spent some time working at primate sanctuaries, and was thinking about going into primatology, but around the time I took this class I was also becoming interested in experimental biology and realized that insects would be a better way to go for taking that sort of approach in my research.

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Photo: H. Woodard

IS: What is your favourite social insect and why?

HW: Bumble bees! The group has it all: they live in some unusual places (like the Arctic), they have solitary and social stages to their life cycle, socially parasitic lineages, unique thermoregulatory capabilities, they’re dominant pollinators in a lot of systems, they buzz pollinate, and so on. I’ll never get bored working on bumble bees. Lately I’ve gotten particularly interested in queen bumble bees, which are just so special because they undergo so many changes (behavioural and physiological) across their life cycle and face so many challenges, like having to survive through the winter and start new nests on their own in the spring before their workers emerge.

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

HW: One of the highlights of my career thus far was going to Alaska for the first time, in summer 2016, to start working with arctic bumble bees. I became fascinated with them when I read Bernd Heinrich’s book Bumblebee Economics as a graduate student and had been wanting to work in that system ever since, so it was gratifying to make that a reality. There is nothing like watching giant Alpinobombus queens fly around open tundra!

2016_Arctic_Bumblebee_24_SN

Searching for Arctic bumblebees.

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

HW: I teach an insect behaviour course for more senior undergraduates and I’m currently developing a new social insects course that I’ll teach for the first time next year, which I’m super excited about. We’re going to talk about theory in the class but I’m also going to heavily emphasize all of the insights we’ve gained through molecular work, especially in the last decade. There’s an awful lot to talk about.

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

HW: The last book I read was Bernd Heinrich’s The Thermal Warriors, which is all about how insects deal with thermoregulatory challenges. It’s a fun read; it takes a complex subject in comparative physiology and makes it very accessible. I highly recommend it, and all of the other books Heinrich has written.

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

HW: E.O. Wilson’s autobiography, Naturalist. I read it the first time in one sitting. Reading it inspired me to go to graduate school and pursue a career in studying social insects. It includes such an interesting treatment of the history of the division between molecular and ecological research, and the idea that that division doesn’t really exist (which Wilson talks about a lot more in Consilience) was exciting to me, given that I was thinking a lot at the time about how to use approaches from molecular biology to study social evolution. Wilson’s passion for ants also really shines through in the book and it’s clear that he appreciates them both for their own sake and because they’re a lens through which you can understand life on Earth, in the broadest sense. That influences how I think about bumble bees: I’m enamoured with them but I also think they contain the answer to every fundamental question in biology.

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

HW: To be perfectly honest I don’t have too many hobbies outside of work, but I have been learning Taekwondo and I’m really liking it. I also love to go hiking and I have three Australian cattle dogs that keep me busy.

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

HW: I experienced burnout at the end of PhD and since then I’ve tried to take it a bit easy on myself and pace myself, when I can. I’ve incorporated more fieldwork into my research program, which gets me out of the lab and office, broadens my perspective, and helps keep me more physically active. I’ve also worked hard to cultivate a buoyant mindset; academia is full of crushing blows to the ego and you have to digest and move on quickly or you’ll get overwhelmed. I also have a lot of wonderful friends in my department who are also new professors and we support each other and celebrate when good things happen.

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

HW: That’s easy, I would bring my dogs, who aren’t ‘things’ to me but I hope would be fair game. They help keep me happy. Hopefully there would also be bumble bees on this island.

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

HW: My PhD advisor, Gene Robinson, has definitely had the greatest influence on my career. When I started graduate school I had a lot of enthusiasm but I didn’t have much research experience and I hadn’t learned how to think like a scientist yet. Gene taught me to think critically, think things through, and think big. I feel so fortunate to have been given the opportunity to learn with and from him.

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

HW: My advice would be to start by picking an organism and learning it well, then the specific research questions will follow. I floundered a bit at first with my bumble bee research because I didn’t really understand them at all – I hadn’t spent time getting to know them, so to speak. Things really picked up for me after I went to Israel to work in Guy Bloch’s lab, where I took a lot of time to sit and watch them, try different things out, and hang out and talk with other bumble bee biologists. The better you know your organism, the better you’re able to formulate solid questions and effectively answer them. All of the best experiments are designed in the context of the organism, in my opinion.