A blog post highlighting the article by Soare et al. in Insectes Sociaux.

By Sean O’Donnell

Army ants are strange beasts. New World army ants (Ecitoninae) share a suite of unusual characteristics, including mass foraging raid behavior, that distinguish them among ants and indeed among all social insects- the army ant syndrome. Their strangeness may breed success: recent evolutionary analyses suggest the army ant syndrome is ancient (perhaps 80 million years old), and army ants are among the most important ecological players in the tropical forests where they thrive.

One component of the army ant syndrome relates to their mode of reproduction. Like some other social insects, notably honeybees (Apis) and some paper wasps (Epiponini), army ant colonies reproduce by swarming. Swarming involves groups of workers and one or more reproductives (queens, in Hymenoptera) moving away from the natal colony to establish a new daughter colony. Army ants are unusual because their impressively large queens are wingless. During periodic bouts of reproduction that occur every few years, an army ant colony produces a single surviving daughter queen who mates with a number of visiting winged males that arrive from distant colonies. After mating, the young queen inherits about half of the worker force and walks away from her natal colony to start a new society.

Differences in mobility between queens and males occur in some ant species and are usually associated with significant sex differences in dispersal distance. In these species of dependent-founding ants, homebody queens settle in or near their natal nests; males fly longer distances to seek mates. This sex difference can be important for population structure: the mobile longer-flying males move genes (alleles) greater distances. It was long assumed that wingless army ant queens were relatively mobility-challenged, and that queens were therefore less important than winged army ant males for maintaining gene flow in army ant populations.

However, another unusual key feature of the army ant syndrome is colony nomadism. Army ants do not dig and occupy permanent nests. Rather, they regularly move or emigrate among a series of temporary shelters where they bivouac, assembling a temporary nest from the interlinked bodies of the workers. In the well-studied species Eciton burchellii, colonies are on a five-week cycle, of which two weeks are spent emigrating among a series of nesting sites. Single emigrations can traverse 100 m linear distance. Successive emigrations tend toward directionality: a right turn on one night’s emigration path is likely to be followed by a left turn the following night. Do such colony movements, summed over the three years between reproductive bouts, contribute to maternal (female) gene flow?

Video of an an Eciton burchellii colony starting to emigrate. Source: S. O’Donnell.

We hypothesized that colony emigrations would contribute to maternal gene flow and reduce or eliminate sex biases in gene dispersal. We tested for sex biases in gene flow by measuring the genetic relatedness among males and females (queens) in a population of the army ant Eciton burchellii parvispinum in the mountains of Costa Rica. We collected samples of workers from a total of 40 colonies in a roughly 10 km X 10 km area. We sampled colonies in the same geographic area in 2006 (25 colonies), and again roughly three years later in 2009 (15 colonies). Three years represents the typical generation time (time between reproductive bouts) for E. burchellii colonies.

We genotyped workers by using PCR primers to amplify seven highly variable microsatellite DNA regions. We then reconstructed the maternal (queen) genotype for each colony as well as the genotypes of the males that had fathered the workers we sampled. We asked whether relatedness among the queens and their mates decreased with distance among the colonies with years, as well as testing for spatial genetic structure between the 2006 and 2009 samples.

We found no significant difference in spatial genetic structure between the sexes, either within or between the 2006 and 2009 samples. In fact, there was some evidence against genetic philopatry for queens: the queens sampled in 2009 were significantly unrelated to queens sampled in 2006 that were collected nearby (within 0.5 km). These patterns suggest maternal dispersal via emigrations contributed to gene flow in these army ants, reducing or eliminating male biases in dispersal. Because colony emigrations summed over the lifetime of army ant queens queen may contribute to gene flow across the landscape. The ecological consequences mean that habitat connectivity is essential to permit colony emigrations and support genetic diversity in populations of this keystone species.

 IS: Who are you and what do you do?

I’m Diana Urcuqui Rojas, I completed my B. Sc in Biology at the Universidad del Valle (Colombia) last year. I love social insects! For my bachelor thesis, I studied the social structure and nest distribution of the ant Gnamptogenys bisulca in four different populations from natural montane forests in Colombia. For this study, I determined nest distribution and composition, and examined differences among castes in terms of morphology (mesosome) and reproductive systems. In this project I also studied the mites hold on the ants, so actually I’m studying mites found inside of G. bisulca nests. I’m also working in little projects and looking for an internship or enrolling in a masters program to continue in this field.

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

My love for social insects started with ants. When I was a biology student I helped another student in her bachelor’s thesis. She was working with nesting strategies of Ectatomma ruidum. That first exposure to ants motivated me to take an elective course named “social insects” with professor Patricia Chacón. This course was fascinating, was awesome to learn about complexes societies between little individuals. I learned about natural history, evolution, ecology, taxonomy and behaviour of ants, termites, bees and wasps. Also we learned some things about some communal insects.  After that, I realized that I wanted to carry on studying social insects.

La Celia – Colombia

IS: What is your favourite social insect and why?

Ants are my favourite, especially army ants, because of their moving colonies and aggressive behaviour. Also, I know the Eciton sp. colonies and I think that their soldiers are so pretty! Moreover, lately, I’m became interested in bees because of their social dynamics (species with individuals living alone and in colonies), which can allowed us to conduct studies that we can’t do with ants.

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

I love the study of natural history and I think that the best moment is when I started my bachelor’s thesis. From that moment I began to see with my own eyes all that I have read about ants, especially how organized a colony can be, how the workers keep the brood’s lives and the morphological differences among the castes. All this was really fascinating and exciting to me. Also, currently I’m really excited because my first publication (Social structure of Gnamptogenys bisulca (Formicidae: Ectatomminae) in tropical forests)!

(Top left) Workers of Gnamptogenys bisulca (Top right) G. bisulca workers with different mesosome. (Bottom) G. bisulca ergatoid with two ocelli

G. bisulca’s nest.

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

Up to now I have taught some things to my close relatives and friends and in one chance, with other biology students, we explained an insects collection to an audience in the library, we had different insects, including an Atta sp. colony. Normally, when I talk about this group, I try to explain some general aspect of their biology that is captivating and similar to humans. It’s awesome when you realized that we have some in commons, we are both social!

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

Regarding Gnamptogenys bisulca, I’m interested in the morphological differences between ergatoids: It would be great to compare what I found (see supplementary material in “Social structure of Gnamptogenys bisulca (Formicidae: Ectatomminae) in tropical forests”) with ergatoids morphology from colonies of other places. Behavioural studies would also be interesting, to analyse how the reproductive queens manipulate the others queens in a colony. Also, I would like to confirm the absence of polydomus in this species.  Concerning other groups, I would like to work with a species that have individuals living in solitary and in groups, and do comparative analyses using different tools (behavioural, natural history and molecular), this would be amazing, I could do it with  bees. I think that any study that make me understand the sociality in a species is interesting to me, I’m open to the possibilities.

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

Those questions related to the origin and evolution of the eusociality in different groups generate the biggest debate. Also, the supercolonies found in some ants open a discussion of what’s a true colony, and therefore, what is the right scale to study these species.  I hope as a result of new research in different species, we can answer these questions in a near future. Moreover, it’s also important to take into consideration the different tools that we have to study social insects, that are equally informative and have a similar likelihood of mistake. Sometimes we just focus in one and think that is the only way to understand something.

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

The last book was “the social conquest of earth”. I think it’s a good book, despite the polemic content, because it’s easily to understand for the general public and its very informative: Wilson explain the eusociality in our species and compares it with the eusociality of social insects.

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

I love spending time with my family, hiking, biking and dancing. I’m learning bellydance and also Indian dance. Moreover, actually I also want to learn somethings about astronomy.

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

I try to be positive all the time. Hard moments always happens to everybody and always you have the option to learn from them, and use them to your advantage for professional and personal growth.

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

Thinking just in surviving I would bring a penknife, a strong rope and a powerful lighter. For me these are the basic elements in a critical situation: with a penknife I can cut different kind of materials, and build others tools. A strong rope is useful to tie up something and keep it together, or drag it, also to build a refuge and to climb a slope. And a lighter to cook, keep warm, and to shoo wilds animals.

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

I have had incredible teachers but my love for social insects wouldn’t be possible without Patricia Chacón, Inge Armbrecht and James Montoya.

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

For me is important to be perseverant, disciplined and goal oriented. I also think that having a second choice is always a good idea.

IS: Who are you and what do you do?

My name is Sean O’Donnell, and it has been since the day I was born. I spend much of my time conducting research that focuses on social insects. Ongoing projects in my lab involve various combinations of thermal physiology, population genetics, community ecology, social interactions/division of labor, and brain plasticity/evolution, working with army ants, theory/equations, dampwood termites, paper wasps, and antbirds. I have dabbled in bumble bees (delightful), leaf cutter ants (bumbling vegetarians), and stingless bees (yes, but they bite). I also teach- in the field and in the tropics as often as possible. I was a Psychology (!) Professor for 15 years until 2011, when I moved to Biology and BEES (Biodiversity Earth & Environmental Science) at Drexel U. in Philadelphia.

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

I didn’t really grow up as a bug-kid; I was more of a broad-ranging junior naturalist, though I have been obsessed (I say healthily so) with Amazonia since age 5. I took AP Biology (on purpose) in high school and majored in Biology in college. A senior thesis project on dragonfly nymph ecology opened my eyes to the wonders of planet insects. After a failed foray into plant population biology graduate work, I found my way to an NSF-funded RA-ship with Bob Jeanne (Wisconsin) to study paper wasps in Costa Rica (to whoever backed out of this position on Bob at the last minute- you have my sincere gratitude!). It was in graduate school that I got my first real exposure to multi-level selection and colony-level adaptations- my conceptual drivers- and I really got hooked on social insects during my 1988 Organization for Tropical Studies course. I did an independent project on Polistes instabilis wasps; I fell hard for wasps and never lost that passion.

IS: What is your favourite social insect and why?

I do have faves, but in different categories. Overall amazingness plus mystery: the army ant Labidus coecus. Joy to watch & collect data upon: Polistes wasps. Cutest: Nectarinella championi wasps. Best nest: Leipomeles dorsata wasps. At the other end of the scale, after working intimately with Solenopsis fire ants recently, I would say they are rather miserable (I still have scars).

Best nest: Red arrow indicates a nest of the paper wasp Leipomeles dorsata on the underside of a leaf blade in Yasuni, Ecuador. The tan area is the dome-like envelope of the nest; note the indented lines, with black material built in, that closely resemble the veins of the supporting leaf.

Cutest: Workers of the paper wasp Nectarinella championi peer from their nest entrance on a tree trunk near Monteverde, Costa Rica.

Joy to work with: Polistes instabilis paper wasps on a newly-founded nest in Guanacaste, Costa Rica.

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

I will never forget the feeling of raw inspiration on the sunny day when I was dining at a Monteverde, Costa Rica Friends’ Meeting potluck many years ago. I was sitting in an open spot enjoying good food and good company, when a small swarm of subterranean Labidus coecus army ants emerged at my feet to grab dropped bits of yummy home-cooked chow. “Wow,” I thought, “army ants really don’t like hot sunny areas. The nearest shade is many meters away. These gals travel underground… I bet doing that buffers them from the sun, and allowed them to get way out here in the open to this food…” My research program is still building on that moment.

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

I regularly work as a field consultant with natural history film productions, most recently in flooded forest in Amazonian Peru. That was an awesome site. I have worked both on- and off-camera with seven different natural history film crews, beginning in 1998. Until my recent fire ant gig, and a cameo with leaf cutters, I have been type-caste (pardon the social insect pun) as an army ant expert. That would be less good if I did not really love army ants, and the tropics. I like to think that the world’s stock of army ant natural history film making would be depauperate if not for my input. The possibility of reaching millions of viewers globally, and awakening their inner army-ant loving fiends, really floats my boat.

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

Well, I won’t give away my hottest current ideas, but it sure seems like social insects are SUPERB systems for analyzing directional climate change effects, from the organism to the ecosystem. I think understanding the interplay of individual physiology and colony performance in varying environments is a fascinating area for exploration. See my recent (20117) theory paper with Kaitlin Baudier on this topic: Current Opinion in Insect Science 22:85-91.

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

A golden oldie…How do we make the evolutionary jump from solitary to obligately social?

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

I just finished Teddy Roosevelt’s 1914 book about exploring an unknown river in Amazonia in the company of the legendary Colonel Rondon (Through the Brazilian Wilderness). I love exploration/travel/adventure writing, and this was a good tale. Some crazy things happened out there in the then-unknown wilds: near-starvation, murder, insane rapids, indigenous people attacking, and it was done by an ex-US president! Who could imagine?

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

I gravitate toward outdoor activities- hiking, birding, canoeing, fishing. I love the ocean and international travel. I also sing bass in a local chorus. I am not much into professional sports, except that I am a rabid life-long Philly sports fan. Hello, Bryce Harper, wake up!

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

I turn to coffee, mostly. And I don’t give up easily; I try to find another angle.

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

1. My family, so they could do most of the work. Or the Darma Initiative staff.
2. Good set of metal tools. Building, harvesting, cutting…
3. Small nuclear sub, in case we decide to leave.

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

My Ph.D. advisor, Robert Jeanne- true wasp expert, skilled writer, careful and critical thinker, patient and inspiring mentor, tropical biologist. Bob also mixes a mean Manhattan.

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

Spend time watching your study animal(s). Observation often pays off in ideas.

A blog post highlighting the article by O’Donnell in Insectes Sociaux.

By Sean O’Donnell

Wasps in the family Vespidae are attractive to social insect researchers because they present nearly the full range of animal social structures, from solitary living species to species with some of the largest, most complex colonies known.  It has long been recognized that some social species of vespid wasps, such as Vespinae (hornets and yellow jackets), have strong caste-related allometry, or differences in body size and shape. Queens and workers are typically distinct to the point that they are readily recognized with the bare eye- there is no need to pull out the micrometer to distinguish a yellow jacket queen from her workers. Some other social vespids also have caste allometry (O’Donnell 1998).

Another potentially fascinating aspect of vespid wasp diversity is the wide range of body sizes exhibited by this group, yet species differences in body allometry in this family seem to have been largely overlooked by researchers.

In a recent pair of studies, my lab explored the evolution of brain versus body allometry among Vespidae species (O’Donnell & Bulova 2017; O’Donnell et al. 2018). We found that smaller species had larger brains relative to their body size. This work inspired me to examine whether vespid wasp species differ in body allometry.

When we analyzed brain-body allometry, we used head capsule volume as our measure of species mean body size. Some reviewers suggested this was not the best approach: what if wasps’ heads varied allometrically with overall body size, and head allometry drove the apparent brain-body patterns? This could happen, for example, if smaller-bodied species had relatively small heads, and their brain size was constant, relative to overall body size. These comments inspired me to test whether wasp head capsule size varied with overall body size. My new findings on wasp head-to-body allometry show that not only were our brain allometry findings supported, they were conservative.

To study head-body allometry, I started by measuring species mean dry weights of the main body trunk (thorax plus abdomen) for the subjects of the brain studies. Because we had photographed the head capsules of the subjects of our brain allometry studies, I had head volume measurements for some species. I added new data and increased the sample size by weighing the head capsules of some of the species for which I had volume data, and I measured both head and body weights for several additional species. I included solitary vespids (potter wasps; Eumeninae), species from the subfamily Vespinae, and species from all tribes of eusocial subfamily Polistinae. The species examined ranged from some of the largest Vespidae (Vespa hornets, and the giant Asian paper wasp Polistes gigas) to some of the smallest swarm-founding Vespidae (Protopolybia and Leipomeles).

Importantly, I found that the two measures of head size, head dry weight and head volume, were tightly isometrically correlated. I then asked how head size varied with body size. All analyses supported a strongly significant negative head-body allometry, in other words, smaller-bodied species had relatively larger heads. This pattern held for head weight, head volume, and when only social species were included in the analysis. I used a special analysis to account for the potential effects of species relatedness on the negative head-body allometry, and the pattern was still highly significant. The magnitude of relative head-size variation was striking: in one of the largest species, head capsule weight approached a mere 5% of body weight, while in a small species, the head comprised nearly 30% of body weight.

Adult female Mischocyttarus sp. (left, a medium-sized species) and Protopolybiaholoxantha (right, a smaller species). I scaled the photos so the wasps appear to be about the same body length, and the relatively large head capsules of the Protopolybia workers are evident. The red scale bars represent approximately 1 cm in each photo.

I believe the strong interspecific head-body allometry in Vespidae is surprising, given that wasps are flying animals. Large heads could affect the wasps’ ability to fly by altering aerodynamics or by shifting the center of gravity. What factors might drive the evolution of allometrically enlarged heads in smaller species?

Our previously published brain size data suggest an answer. Remember that brain size relative to head size increased as smaller body size evolved. Since we now know that smaller wasps also have relatively larger heads, this means that the negative allometry of vespid brain size outpaces the negative allometry of head size. In other words, smaller species’ brains make up an ever-increasing portion of their relatively larger heads. Again, variation in the magnitude of brain size to head size was dramatic: brain volumes ranged from about 2% of head volume in the largest species, up to 12% of head volume in the smallest species.

In other vertebrate and arthropod lineages, the relatively large brains of the smallest species are associated with modification of heads including thinning of skulls (vertebrates) or head capsule walls (arthropods), and with reductions and bodily displacements of tissues such as muscles. Have the relatively large brains of vespid wasps driven similar changes in head capsule structure or physiology? Perhaps the need to house large brains has affected the behavior and ecology of small vespid wasps: limits on head musculature or head cuticle thickness might limit the wasps’ abilities to bite and chew building materials or food. If so, the need to house relatively large brains could set biomechanical lower limits on body size evolution in the family.

 References

O’Donnell S (1998) Reproductive caste determination in eusocial wasps (Hymenoptera: Vespidae). Annual Review of Entomology 43:323-346.

O’Donnell S, Bulova SJ (2017) Development and evolution of brain allometry in wasps (Vespidae): Size, ecology and sociality. Current Opinion in Insect Science 22:54-61.

O’Donnell S, Bulova SJ, Barrett M, Fiocca K (2018) Size constraints and sensory adaptations affect mosaic brain evolution (paper wasps- Vespidae: Epiponini). Biological Journal of the Linnean Society 123:302-310.

IS: Who are you and what do you do?

My name is Mariane Ronque and I recently finished my PhD. in Ecology at the University of Campinas (Brazil). Using a multidisciplinary approach, I investigated the natural history, behaviour, and associated bacterial community of five species of fungus-farming ants from the Atlantic rainforest, with a special interest in non-leafcutters: Mycocepurus smithii, Mycetarotes parallelus, Mycetophylax morschi, Sericomyrmex parvulus and Sericomyrmex saussurei.

(left) Nest of Mycetophylax morschi in Atlantic rainforest; (right) Fungus garden of Sericomyrmex parallelus.

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

I always had an interest in behavioural ecology and species interactions, beginning in my undergraduate studies. Ants became my interest because I wanted to study behavioural ecology and species interaction in a masters course, so I started to read a lot about these themes during my undergrad. When I was reading research about ant social organisation, how they participate in interactions with other arthropods and plants and acting on the dispersion of seeds, I became fascinated and recognised that they would be good models to study behavioural ecology and species interactions.

IS: What is your favourite social insect and why?

Ants, probably this answer is biased because I study ants! But I think ants are a good model to study social behaviour and ecological interactions. In addition, the variety of behaviours, ways of life and abundance in terrestrial environments fascinate me.

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

In my PhD when I observed in the field the behavior of cleptobiosis in fungus-farming ants (see the video below). It was very cool to watch Mycetarotes parallelus steal faeces pellets (probably to cultivate the symbiont fungus) from Mycetophylax morschi. I got very excited when I realized that probably this was the first record of cleptobiosis in fungus-farming ants. I reported this behavior in a recent paper at Insectes Sociaux – Thievery in rainforest fungus-growing ants: interspecific assault on culturing material at nest entrance, (Ronque M.U.V., Migliorini G.H., Oliveira P.S., 2018).

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

A question that I am currently interested in is how the associated microorganisms (microbiota) shapes the social behavior in ants. There has been an increase in the interest in the microbiome associated with animals since microorganisms are very abundant and some can affect animal ecology, evolution, and behavior. There is research showing that microorganisms can shape some social behaviors in meerkats, chimpanzees, hyenas. I would like to see this area of research expanding in ants since they are social animals that live in colonies and microorganisms could have key functions in the ant’s societies.

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

I like to cook, travel, be with my family and my partner.

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

I try to stop a while and give myself a time to relax. Talking to my partner and parents also help me to see the situation more clearly and think strategically to solve the problem.

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

This is a difficult question! Based on what I see in survival TV shows, I think it would take a fishing net, a knife, and a pot to boil water. Cannot it be 4 things? Because I would also need someone to share the experience, so I would bring my partner that is an ecologist with expertise in the field and would help me to survive on this island.

Me and my partner collecting nests of fungus-farming ants (Brazilian Cerrado).

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

My graduate advisor Dr. Paulo S. Oliveira. It was in his laboratory and under his supervision that I started studying ants during my master course. He showed me the importance of natural history studies to understand the ecological role of the organism in the environment in which it lives, as well as being the first step in formulating more detailed questions about a species and the interactions in which it participates. I also cannot fail to mention my parents, who always encouraged me to continue in my science career.

Me and my advisor Dr. Paulo S. Oliveira during poster presentation at IUSSI 2018 – Guarujá.

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

Be passionate about your research and scientific career. Be kind to yourself, sometimes things do not go as expected and we should not charge ourselves so much. Try to know the maximum of the organism or the system you study (as field and lab observations), this will allow more in-depth questions. Also, I think it is very important to learn new technologies (especially molecular tools), experimental design and statistic.

A blog post highlighting the article  by Yong, Matile-Ferrero and Peeters in Insectes Sociaux.

By Christian Peeters

Many ant genera obtain honeydew from a variety of scale insects feeding on the sap of tropical trees. However, the most advanced and speciose scale insects – family Diaspididae – do not excrete honeydew, but build a protective shield made of wax and proteins and are known to associate with only one ant genus in Africa and Madagascar. The minute workers of Melissotarsus chew an extensive network of tunnels under living bark, and these are inhabited by vast numbers of diaspidids. Typically, these do not secrete the trademark shield when defended by ants, unlike free-living forms. Melissotarsus workers have extremely modified legs and cannot walk outside host trees, it is therefore assumed that they obtain all their food from the scale insects.

The Asian genus Rhopalomastix is strikingly similar in morphology to Melissotarsus, especially the bullet-shaped head of workers with the antennal sockets touching each other (in all other Myrmicinae, the antennal sockets are widely separated), and silk glands inside the head of adult females. However, the legs are normal, and a sting is retained. Molecular data confirm these are sister genera, sitting together on a separate branch. Rhopalomastix is widely distributed (India to eastern Australia), yet its biology was undocumented until Gordon Yong located it in Singapore. Four species nested in seven genera of living trees, together with five genera (one new) of diaspidids. Large numbers of naked diaspidids occurred in all ant nests, with only few shields.

Heads of Melissotarsus and Rhopalomastix workers, showing how the antennal sockets meet in the center of the face (SEMs by Roberto Keller). Note that the Melissotarsus mandibles are strikingly abraded, indicating an old individual. The ventral expansion of the head accommodates large opener mandible muscles, a novel adaptation for chewing through healthy wood (Khalife et al. 2018). Image: Roberto A. Keller/AMNH

This mutualism is distinct from others involving ants and scale insects because of striking differences in the biology of diaspidids: (i) they feed on parenchyma cells, not the sap; (ii) adults are strictly sessile. First instars (‘crawlers’) disperse but once they have selected a feeding spot and insert their stylets, the legs and antennae degenerate. Thus, ants cannot regulate the distribution of diaspidids within their tunnels, instead the crawlers decide! Ant eggs are distributed throughout the tunnels and larvae feed autonomously, a character also found in attine ants where larvae feed on the cultivated fungus. We lack direct observations of feeding behaviour because the ants switch to other tasks once we exposed the tunnels. Do they eat the flesh of diaspidids? Or their milk (secretions of wax and proteins normally used to build the shield)? Probably both. Diaspidid exuviae are not found in the tunnels, suggesting that they are also eaten by the ants.

Naked diaspidids (Andaspis numerata) and a few shields (green arrows) inside Rhopalomastix tunnels.

Trees hosting ants and scale insects generally benefit because the cost incurred from the ingestion of sap is compensated by the protection given by ants against leaf herbivores. This is not so in the mutualisms involving diaspidids with Melissotarsus and Rhopalomastix, because these ants are unsuited to be guards. Indeed, after removing bark and exposing tunnels, we observed that both workers and brood were preyed upon by Pheidole and Crematogaster ants. Field studies need to determine what is the impact on host trees, especially in fruit plantations (mangoes, durians, …) that are often preferred. Because only older trees are infested, we assume that these are more tolerant of the diaspidid exactions. Of special note is the host tree Aquilaria that is harvested commercially to produce an extremely valuable resin used for perfumes.

Numerous naked diaspidids in galleries of Rhopalomastix from Thailand. Ant larvae are scattered along the tunnels.

Rhopalomastix is likely to be widespread throughout tropical Asia but it is necessary to scrape tree bark with a knife in order to locate nests. Previous collection events were restricted to pyrethroid spraying of tree trunks, and soil pit traps (hence they are often classified as ‘litter ants’). We have recently found their arboreal nests in Thailand, Borneo and the southerly Japanese island of Okinawa.

Gordon Yong investigating a nest of Rhopalomastix on mango tree (Pulau Tekukor island, off Singapore).

References

Khalife A, Keller R, Billen J, Hita Garcia F, Economo E & Peeters C (2018) Skeletomuscular adaptations of head and legs of Melissotarsus ants for tunnelling through living wood. Frontiers in Zoology 15: 30.

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).

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.

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.

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.