Red wood ants stalked by a Trojan horse

Highlighting upcoming research from Thomas Parmentier entitled ‘Host following of an ant associate during nest relocation’, to be published shortly in Insectes Sociaux

Even more fascinating than ants, is the extremely diverse group of arthropods that live strictly in their nests. Gradually, we learn that these creatures, commonly  referred to as myrmecophiles or ‘ant loving’, possess an array of chemical, morphological and behavioural adaptations to by-pass ant aggression and to make a living in the hostile nest environment (Kronauer and Pierce 2011). Many myrmecophiles are parasites that feast on a lavish banquet of brood and other resources found in the nest (Parmentier et al. 2016a).

What is rather unknown so far, is how myrmecophiles move in the landscape and target new nests. It can be expected that myrmecophiles are prompted to colonize new nests, when nest conditions start to deteriorate or when competition with other myrmecophiles becomes too strong. During my current postdoc project, I study the spatial dynamics of myrmecophiles associated with European red wood ants. These ants are famous for their large mound nests and aggression, yet their nests harbour a rich community of myrmecophiles (Parmentier et al. 2014).

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Last spring, I visited a study site in the north of Belgium and to find out whether the wood ant colonies (Formica polyctena) made it through the winter and whether new nests were founded. Then, I observed that one colony was moving to a new nest site a couple of metres away. As I have been curious for a long time how myrmecophiles would respond to the desertion of their home, I carefully inspected the horde of moving workers. To my surprise, I saw that a group of larvae of the beetle Clytra quadripunctata (Chrysomelidae) were crawling among the moving colony towards the new nest site. A bit later, some larvae were also dragged by the workers to the new nest. Luckily, these days, smartphones are equipped with rather decent cameras, so I was able to record this rare event. There are some old and anecdotal notes which suggest that some myrmecophiles are also able to track their host during relocations to a new permanent nest site, but this has not been recorded so far.

The biology of Clytra quadripunctata is rather peculiar. The adults are adorable beetles that feed on plants near the nest. After mating, the female drops her eggs. The larvae enter the nest and remain there probably for 2 years (Donisthorpe 1902). Lab tests demonstrated that the larvae are brood predators and scavengers. They preferentially reside in the heated brood chambers in the centre of the nest (Parmentier et al. 2016b). The larvae of this beetle are protected by a pear-shaped case in which they can retract. After pupation, the adults sneak out of the ant nest.

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My observations suggest that the beetle larvae adaptively respond to rare nest-moving events. Interestingly, they can find the new nest site on their own or be carried by workers unaware of the danger that is hiding in the case. Nonetheless, a significant fraction of the larvae did not find the new nest and remained in the abandoned nest. Wood ants are thought to move occasionally when microclimatic conditions become suboptimal. However, they may also be triggered to relocate to a new nest site in order to reduce parasite load. This could end up in an evolutionary arms race where the host will move more frequently and more distantly, whereas the parasite will develop more advanced strategies to follow or locate its host. This is a tempting hypothesis that deserves further research.

This observation has galvanized me to unravel some more secrets of myrmecophile dispersal the coming years. More information on the progress of my research on myrmecophiles can be found at:

https://www.researchgate.net/profile/Thomas_Parmentier

 

Donisthorpe HSJK (1902) II. The Life History of Clythra quadripunctata, L. Trans R Entomol Soc London 50:11–24.

Kronauer DJC, Pierce NE (2011) Myrmecophiles. Curr Biol 21:208–209.

Parmentier T, Dekoninck W, Wenseleers T (2014) A highly diverse microcosm in a hostile world: a review on the associates of red wood ants (Formica rufa group). Insectes Soc 61:229–237.

Parmentier T, Bouillon S, Dekoninck W, Wenseleers T (2016a) Trophic interactions in an ant nest microcosm: a combined experimental and stable isotope (δ13C/δ15N) approach. Oikos 125:1182–1192

Parmentier T, Dekoninck W, Wenseleers T (2016b) Do well-integrated species of an inquiline community have a lower brood predation tendency? A test using red wood ant myrmecophiles. BMC Evol Biol 16:12.

 

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

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.