Why are wee wasps big-headed?

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.

 

Interview with a social insect scientist: Graham Birch

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IS: Who are you and what do you do?

GB: My name’s Graham. I’m a master’s graduate from the University of Exeter, coming to the end of a year working as a volunteer research assistant in South Africa for the Kalahari Meerkat Project. I’ll be starting a Ph.D. back at Exeter in September on Banded Mongooses.

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

GB: I’ve always been interested in sociality and how it’s evolved, and ants specifically can form such huge and complex groups, with multiple distinct castes. Many species are intensely territorial, with group size and make-up largely determining success; therefore, conflict may have been a significant driver in the evolution of ant societies. But the threat of competition is not necessarily ever-present and being ready for battle all the time may be wasteful, so an intriguing question is whether coordination and behaviour of these complex groups can plastically respond to the level of threat in the local environment in response to cues, which is the subject of our paper.

IS: What is your favourite social insect and why?

GB: Termites moult multiple times before reaching their adult forms, but some primitive species can moult backward in time to a younger form! They’re therefore able to plastically change their development in response to the colony running out of resources. They can also switch development between different castes if they like to a certain extent, which I just find super cool.

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

GB: I haven’t done too much of my own research so far, but I (but mostly my dad) did start a meme where scientists left Amazon reviews for items they used in their research (but not based on the intended purpose). Started when we had the idea of using tea strainers to protect ants we introduced into another colony, and my dad left a review about how great a capsule for ants these tea strainers were (anything to get his ranking up!), which the tea drinking public found a bit odd/hilarious. It became the top review, started a twitter trend of other scientists leaving similar reviews, which got picked up by The Washington Post (easy to find on Google!). I even did a couple of phone interviews. It was all very surreal but definitely memorable!

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

GB: Again it’s a bit early in my career to answer this question, but I have lead turtle conservation tours in North Cyprus, and Meerkat research tours in the Kalahari, which did involve communicating the science of what we were doing to the public. I hope to do some demonstrating and maybe teaching during my Ph.D.

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

GB: Broadly the big issue, not just for social insects, is climate change. Does the level of sociality mean these species are more able to shift their ranges or, if they can’t, can they deal with new competitors or enemies that can (as well as changes in temperature itself), over other less social species?

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

GB: I fear I may be a bit naive at my career stage and may not have enough experience on social insect research generally (beyond group conflict) to comment on this. However, what I have found to be controversial is the definition of eusocial when looking at non-insect taxa. For example, there was a lot of buzz about naked mole rats being the first eusocial mammal due to their large groups and division of labour among reproductives and workers, but recently many have turned against this. You could even say the same for humans where, even though we don’t have fixed caste determination, we have orders of magnitude larger and more complex societies then eusocial insects in terms of numbers and the division of labour we see in the variety of jobs we can pursue. Maybe it’s just unhelpful to use the term for non-insects.

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

GB: Ultrasociety. Phenomenal book looking at how human societies have changed and evolved from egalitarian hunter-gathers to incredibly unequal archaic societies led by God kings, to how religion and war shape these into the relatively more equal modern societies we see today.

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

GB: Badminton, swimming, diving, and travelling.

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

GB: Try to not have your research as the only focus taking up all of your time. Get involved in a sport, volunteer, or just something to focus on that isn’t science / your degree, so when you do get stuck you have something else to work on that refreshes you for when you come back to your science.

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

GB: Anyone at the Kalahari Meerkat project, or who went with me on my expedition to Madagascar over a year ago, can vouch for me when I say I’ve almost already done this, but on the island of an isolated research base (days of travelling away from the nearest major town with no communication with the outside world in the case of Madagascar). Anyways, I’d bring a Kindle with a vast library of books so I can read to pass the time, a snorkel and fins (since I’m on an island I might as well enjoy the marine life), and a Camelback so that I don’t have to carry a water bottle around in my hands.

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

GB: Again, I’m very early into my career, BUT I would have picked a Natural Science degree rather than Zoology at Exeter if I hadn’t read the Selfish Gene and Extended Phenotype during the summer before year 11. This made me incredibly passionate about evolution, especially of behavioural strategies. I am so thankful I made that decision, so for that alone, Richard Dawkins.

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

GB: Well, I’m not exactly old myself… but just read some books about behavioural ecology/evolution and see if you get hooked. If you do and find yourself on a zoology or similar degree, read up on the profiles/publications of all of the lecturers at your university and seek the ones that share your interests / get involved! Do this early, and you may be working with them on your thesis later on and perhaps beyond.

Interview with a social insect scientist: Anindita Brahma

Anindita Brahma (2)

IS: Who are you and what do you do?

AB: I am Anindita Brahma, recently completed Ph.D. from Indian Institute of Science, Bangalore, and currently I am a Marie Sklodowska-Curie postdoctoral fellow at Queen Mary University of London. My primary research interest is understanding the proximate and ultimate causes of the evolution of social behaviour.

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

AB: I developed a general liking for animal behaviour during my college days as a bachelor’s student. During my master’s studies at the University of Calcutta, my mentor gifted me a book named ‘Survival Strategies’ by Raghavendra Gadagkar. This book changed my perspective about studying animal behaviour, especially social behaviour, and it deterred me from almost plunging into immunology. I became curious about the author and his works, and a few months down the line I ended up joining his lab as a Ph.D. student. 

IS: What is your favourite social insect and why?

AB: Well, although recently I have started working on ants, wasps were my first love. They are such a fascinating combination of beauty and danger (because their sting is excruciating!), and I find their social behaviour intriguing, especially that of the non-temperate primitively eusocial ones. Also, my Ph.D. thesis revolved around a primitively eusocial wasp (Ropalidia marginata), and maybe because of this, wasps will always have a soft spot in my heart. However, I am now venturing into the world of ants, and I am looking forward to investigating and learning many exciting and awe-inspiring things about them.

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

AB: My entire Ph.D. was quite eventful. However, by far, the best moment has been the time when I was running an experiment to understand the dynamics of gaining direct fitness through natural nest foundation by workers of the Ropalidia marginata. One beautiful day during my daily behavioural observations, I saw that some workers had aggregated outside the nest and involved in aggressive interactions, after which they returned to their nests and behaved “normally”. Soon, a few of the aggregating wasps left their nest and initiated a new nest together. That was a ‘eureka moment’ for me as before this we had no idea that worker wasps interact and plan to leave the nest way before they actually leave it. Moreover, now I can proudly say that such shrewd planning would put any politician to shame!

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

AB: During my Ph.D., I taught animal behaviour to undergraduate students, and I used love answering all the interesting queries they had about the ways of life in the animal kingdom. I also love to explain my research to my friends, acquaintances, school and college students, many of whom do not have the faintest idea about animal behaviour and evolutionary biology. I find it essential to use simple language without any technical jargon and provide analogies and relatable examples from day-to-day life to make research ideas more accessible.

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

AB: I think the current important questions in social insect research are related to understanding the evolution of eusociality. The transition from solitary ancestors to a social form and the successful maintenance of this derived social form still has many mysteries that are yet to be unfolded. For this, we need to have a holistic approach, and I think that it can be achieved by combining carefully-designed behavioural experiments with molecular tools and computational techniques.

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

AB: I think one of the biggest debates in social insect research is still the one started by Martin Nowak, Corina Tarnita, and E.O. Wilson with their paper on the evolution of eusociality (Nowak, M.A, Tarnita, C.E and Wilson E.O. 2010. The evolution of eusociality. Nature. 466 pp 1057-106). The authors of this particular paper claimed that the haplodiploidy hypothesis (which has been the basis for sociobiology research for decades) has failed and that the focus has been given to the relatedness (r) part of the r>b/c inequality compared to the benefit and cost parts. They go on to claim that the kin selection theory is not a general one, doesn’t provide much biological insight, and that standard and much simpler natural selection models are adequate to explain altruistic behaviour. Following the publication of this article, there have been vigorous debates among the social insect researchers on the question of the importance and necessity of W.D. Hamilton’s theory of inclusive fitness. As a matter of fact, there has been a series of interesting commentaries (links to these commentaries are provided at the end of this post) on this issue portraying that Nowak et al.has indeed provoked social insect researchers everywhere.

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

AB: I recently finished reading ‘Gene Machine: The Race to Decipher the Secrets of the Ribosome’ by the Nobel Laureate, Venki Ramakrishnan. This book is a memoir of his research life and his contribution to unravelling the structure of the ribosome, and he describes what does it mean to “do scientific research”. I found this book fascinating as it takes you through the journey of a researcher’s life, which is no less than a roller-coaster ride. The book describes the frustrations and struggles in the life of a researcher as well as the little joys and the rare ‘eureka moments’ that motivate a researcher to strive on and dig deeper to try and understand a phenomenon. Moreover, his informal and witty writing style is something that makes this book relatable. I would strongly recommend that everyone read this book and take a moment to ponder the nature of science and scientific research.

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

AB: I love to read all kinds of fiction and non-fiction books, and my idea of a perfect lazy day is a book and a hot cup to tea. Another passion of mine is music. I have been trained in Hindustani classical music since childhood, and I love listening to a wide variety of music and sing whenever I find the time. 

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

AB: When things get tough (which is quite a common scenario in research life), I think about the little moments of joy and laughter, a few incidents that motivates me not to give up, and try to calm down and focus. Also, if these do not work out, then I have always found that speaking my heart out to a friend and/or a mentor helps me to a great extent! 

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

AB: 1) Drinking water, 2) a tent, and 3) books (lots and lots!). Drinking water because I would not survive without that, tent for shelter, and books because there cannot be a better way to spend time when one gets to stay away from civilisation.

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

AB: This person is undoubtedly my Ph.D. supervisor, Prof Raghavendra Gadagkar. He has been an inspiration throughout, and I could not have asked for a better mentor. Not only did I learn the basics and ethics of scientific research from him but also that research is not about costly equipment, but the logic behind framing a question and the elegant and detailed design of an experiment.

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

AB: Social insects are elegant and unusual. Some of them may not look “cute” in the first instance but believe me, once you start knowing them, they will reveal a whole new world of intelligence in front of you and will amaze you every step of the way. Working with social insects requires much patience, but at the end of the day when you observe them or even maintain them and care for them, it gives you an immense sense of satisfaction.

Links to the Commentaries

Sociobiology in turmoil again

Inclusive fitness theory and eusociality

Kin selection and eusociality

Only full-sibling families evolved eusociality

Inclusive fitness in evolution

In defense of inclusive fitness theory

Nowak et al. reply

Interview with a social insect scientist: Mariane Ronque

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.

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(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 SociauxThievery 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.

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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.

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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.

Interview with a social insect scientist: Nathan Lecocq de Pletincx

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IS: Who are you and what do you do?

NLP: My name is Nathan Lecocq de Pletincx. I am a Ph.D. student in the Evolutionary Biology and Ecology unit of the ULB (Université Libre de Bruxelles). I am working in the group of Serge Aron on the evolution of reproductive strategies in ants. More specifically, my research focuses on population and colony genetic structure in connection with the hymenopteran sex determination system.

 

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Two Ocymyrmex robustior workers interacting outside the nest.

 

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

NLP: I have always been interested in the origin and evolution of sociality. Watching documentaries on a great diversity of social animals, I discovered how fascinating their behaviour is. Later, I developed a keen interest in reproductive strategies after learning the existence of original primary modes of reproduction (queen thelytoky, hybridogenesis, etc.) in several ant species. As Hymenoptera combines sociality and a great diversity of reproductive strategies, I decided to work on this biological model for my Ph.D.

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Ovaries of a non-mated ergatoid queen, showing active ovaries with ovules, yellow bodies, and an empty but swollen spermatheca.

 

IS: What is your favorite social insect and why?

NLP: Ants are fascinating models to study the causes and consequences of sociality and reproductive strategies. In fact, social structure, dispersal strategy, mode of reproduction, ecology, and mode of sex determination are so many characteristics that can interact directly or indirectly and vary significantly between species. Further, studying the causes and consequences of all these features is facilitated by the ease to rear and manipulate ants in the lab.

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A worker of Ocymyrmex robustiorat the entrance of the nest.

 

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

NLP: I think the evolution of cooperation and of its most complex form, eusociality, has yet to be better understood. Numerous ‘mathematical’ models detailing the mechanisms at the origin of cooperation and eusociality have been proposed. In my opinion, it would be interesting to test these hypotheses ‘on the biological side’. Finding species matching our needs is essential to future research. On the other hand, the consequences and correlates of cooperation and eusociality have been better studied. However, there is still a lot to do, especially in the field of molecular genetics. Pursuing the development of molecular techniques and tools to analyse big data sets is crucial for future research.

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

NLP: I practice athletics a lot and bike regularly. I also like to read and learn new things about training methodology in sport. Spending time with my family is also of great importance to me.

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

NLP: For me, the best way to pass through difficult periods is by doing sport. There is no better way to relax than to train hard and go home with the feeling of having had a good session.

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

NLP: I think teachers are of great importance because the way they teach influences and helps shaping our vision of the different topics we study. The animal behaviour, genetics, and molecular and cell biology courses I have taken have had a great impact on my way of thinking.

Rhopalomastix ants feed on diaspidid scale insects inside living trees

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.

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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.

Picture1

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.

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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.

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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.

 

Accessing the file drawer of experienced researchers: joint interviews with Bert Hölldobler and Robert Page

Every day, thousands of papers in various research fields are published. Some of them receive lots of attention, while others remain unnoticed. Simultaneously, thousands of studies are not even submitted to journals because the results are insignificant or the authors think the work does not add sufficient new knowledge to their research field. In these joint interviews by Insectes Sociaux and Myrmecological News, Bert Hölldobler and Robert E. Page Jr. share some interesting insight about their own research and why some studies did not result in papers. Here, you will read the interview with Dr. Robert Page. Also, check out the corresponding interview with Dr. Bert Hölldobler!

Founders Day-Robert Page

IS: Dr. Page, as you look back on (and are still proceeding with) a fantastic career in social insect research, roughly how many papers have you published so far?

RP: I have published about 250 papers so far, including reviews and book chapters.

IS: Which of your papers received the most widespread attention? Did you expect this?

RP: The honey bee genome sequence paper in Nature in 2006 is by far the most cited, but I was one of a million authors, and it is basically a resource paper. I expected it to be the most cited.   Next is the Cell paper I published with Martin Beye in 2003.  I also expected it to be cited a lot because it is probably the most important paper I’ve been a part of.  It also represents a long hard struggle in my lab and Martin’s spanning about 7 years, and a question I actually started working on in 1980.  My 4thmost cited paper is one I published in Experimental Gerontology with Christine Peng in 2001.  It was a review article on a subject I knew little about but was picked up and has been cited 300 times.  I never would have figured that.

IS: Have you published any papers that you think received insufficient attention from the scientific community? If so, can you give us an example?

RP: I have several, but I know why they didn’t receive the attention I thought they should.  I tend to undersell my work.  I don’t go for high impact journals, just because they are high impact.  I try to publish in the journal that is appropriate for the audience I am trying to reach.  Often that is an audience of specialists.  I also tend to publish places that let me present all of the data and methods.  In the long run, the ability to repeat someone else’s work is the hallmark of science, and you need to provide your data.  And, hypotheses and current trends in what is perceived as exciting science come and go, but bad data stand forever.  So, I try to present all of the data as best I can so they can stand whether my ideas do or not.

IS: What do you think is the main reason well-designed studies go unnoticed by the scientific community?

RP: Science today is like a collection of infomercials.  If you don’t package it right and sell it in the right venue, it goes unnoticed.  I guess I am an old fogey about this, but I believe it.

IS: Have you completed studies of which you have not published the results even though you consider them relevant? To how many projects or datasets does this apply over your career, approximately?

RP: Yes of course. I don’t believe in “do an experiment, write a paper.”  The objective of science in my mind is to contribute to an understanding of something. Sometimes experimental results obfuscate our understanding, not improve it.  Usually, more experimentation will fit the pieces together and lead to an understanding, but sometimes you don’t get back to it, so it sits in the filing cabinet, or in an electronic file on your computer desktop.  I have many incomplete studies sitting there.

IS: Do your unpublished datasets have anything in common? Why did you not publish them? Was it ever due to a lack of statistical significance?

RP: As I said in the previous question, it is usually because I can’t figure out how the results fit into a bigger understanding.

IS: Does the field of social insect research generally suffer from gaps due to data not being published?

RP: No, I think too much is published too soon.  We would be better off with fewer papers that actually resolve something.

IS: What do you think is the general trend over time concerning the amount of unpublished data? Stable, decreasing, increasing?

RP: I really don’t know about other people.  I think mine increased over time because as I got older and had more of a focus on specific questions that I wanted to answer, I became more demanding that each paper contributed to an understanding.

IS: Would you be willing to share any or all of these unpublished data so that others could learn from them or profit in any other way? If so, what might be a good platform for this? Do you think that, for example, a database could be set up for such data?

RP: That is a difficult question.  My idea about bad data lasting forever actually came from Darwin.  Often there are reasons data don’t get published, often it is a lack of confidence in them.  Something peculiar in the methods, or an environmental anomaly when the experiment was conducted.  I don’t think any data should be shared on a public platform that isn’t completely reliable and carefully screened.  If you do that, you should write the paper.

Book Review: The Ants of Central and North Europe

By Heike Feldhaar (University of Bayreuth, Germany)

Seifert Ants of Central and North Europe

Many people are fascinated by ants and their behaviour. Even children will often recognize these little busy-bodies that always seem to be determined to pursue their work. Ants have captured the attention of many hobby entomologists. At least in temperate regions of the world, they are an attractive and manageable group in terms of species number. However, species identification of ants is often difficult; in comparison to other insects, ants have seemingly fewer characters for easy identification, such as colour patterns of butterflies or bumblebees. Several ant genera, such as the Holarctic Lasius, Myrmica, or Formica, contain species that even professional myrmecologists have trouble identifying. Only a few very conspicuous ant species, such as Dolichoderus quadripunctatus or Lasius fuliginosus can be identified easily without magnifying glasses; many require some type of optical equipment. In the field, notes on the structure of nests or habitat features help to narrow down species identity.

A good guidebook should, therefore, include a workable key for species identification as well as an informative natural history section with detailed pictures. Bernhard Seifert’s The Ants of Central and North Europe (2018) provides precisely that. The book is divided into two major parts: a “General Part“ with an overview of ant natural history and ecology, and a “Special Part” with a key to all 180 species (for gynes and workers) occurring outdoors in Central and Northern Europe (and a few more that may expand their range into the region) and detailed natural history information for every species. Here, I describe the contents of these two parts in more detail.

The “General Part” (translated into English by Elva Robinson) comprises short chapters on the general morphology of ants, ecological aspects such as their habitats and nests, colony foundation and life cycles of colonies, social parasitism, natural enemies of ants, and feeding strategies. These feeding strategies include interactions of ants with trophobionts for honeydew consumption and seed dispersal by ants. This general part may be skipped by professional myrmecologists that are familiar with the general biology of ants and the corresponding terminology. For beginners, it lays the foundation for understanding the “Special Part” in which Seifert provides natural history details for every species.

The “Special Part” begins with a short introduction to ant determination and mounting, a list of the covered ant species (with a focus on Germany, Switzerland, Austria and South Tyrolia), a checklist of German ants with information on their distribution within Germany (occurrence in federal states, vulnerability and broad ecological niche), and an overview of their ecological preferences and tolerances. This table covers ~ 90 of the 180 ant species and is based on over 200 plots studied by Seifert in Central Europe during the years 1979–2015. It provides detailed information on temperature and humidity preferences and occurrence patterns with respect to plant cover. Thus, the three tables focus on the area where Seifert was most active himself, and less information is available on other areas of the geographic range covered in the book, such as Fennoscandia, Great Britain or Northern France. However, Seifert lists occurrences and ecology of species in these areas in the detailed species accounts. This part is followed by three short chapters where Seifert discusses methods of taxonomic delimitation of species (morphology vs. genetics), justifies the method used by him, numeric morphology-based alpha-taxonomy (NUMOBAT), and defends Linnean binomial nomenclature. These three chapters are part of an ongoing debate among taxonomists, and amateur myrmecologists will most likely skip these four pages.

Seifert then provides an identification key from subfamily to species level (for gynes and workers) for the 180 ant species with outdoor occurrence and nine Mediterranean species that will likely expand their range into Central and Northern Europe due to climate warming. Tramp species are also included, which are mostly found in warm buildings such as larger greenhouses. The key is illustrated with line drawings for many characters that allow for easy comparison of different character states. These drawings might be challenging for beginners, such as the detailed drawings of antennal scapes viewed from different angles of Myrmica workers, but once the reader has grasped the concept, these drawings are very helpful and allow identification to species level. The key works well for slightly advanced ant enthusiasts for the majority of species. For a few species, optical equipment with a micrometer is required; this will not be available to most amateurs, but this is a hurdle in all insect groups and not a failing of this book.

The key is followed by a detailed description of the life histories and profiles of all ant species covered in the book. Bernhard Seifert provides detailed information on the geographic range, habitat and ecology, abundance and nest structure, colony demography and population structure, as well as nutrition and behavior of all species (if known!). These natural history notes are beneficial to beginners and professionals alike. They contain most of the basic information known for each species and are referenced very well, which allows an interested reader to quickly find more details for each species (the reference section contains more than 1,000 references!). Thus, the book is a great starting point for myrmecologists who want to know about the natural history of a particular ant species. The life history and reference sections are substantially extended in comparison to the German book Die Ameisen Mittel- und Nordeuropas, which appeared in 2007 (Lutra Verlags- und Vertriebsgesellschaft), making it not a mere translation of the former.

Students, amateur myrmecologists, and specialists will appreciate Bernhard Seifert’s The Ants of Central and North Europe. The “General Part” provides an excellent overview of general ant ecology and natural history to enthuse amateur myrmecologists, whereas the keys might be challenging for beginners but are very helpful for specialists as they allow the identification of most ant species occurring in Central and North Europe. The extensive information on each ant species makes it an essential reference about ants in this geographic region for all interested readers – from beginners wanting to know more about ants to professional myrmecologists.

 

SAMSUNG CSC

Heike Feldhaar

 

Reference

Seifert, B. 2018. The Ants of Central and North Europe. – lutra Verlags – und Vertriebsgesellschaft, Tauer, Germany, 408 pp; ISBN 9783936412079 (hardcover), EU € 64.00.

In termites, the evolution of alate body size caught between two opposing selective forces

A blog post highlighting the article by T. Chouvenc in Insectes Sociaux

By Thomas Chouvenc

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Alates of Coptotermes gestroi emerging during a dispersal flight event, with soldiers guarding the exit holes.

Sexual selection and partner choice have been hot topics in behavioral ecology over the past few decades, as scientists have been investigating impressive cases of sexual dimorphism and extreme attributes both in vertebrates and arthropods. In some social Hymenoptera, the males are often reduced in size and function compared their female counterparts. The need for a massive accumulation of metabolic reserves in these males has decreased over evolutionary time as their role has been reduced to simple yet functional sperm missiles. In termites, such extreme reduction of the male size is not present (despite cases of significant sexual dimorphism): both the female and male are essential during colony foundation as they provide exclusive monogamous biparental care within the first few months of the life of the colony. The royal couple will then spend years, sometimes decades together, contributing solely to reproduction. One might argue that such lifestyle should promote the evolution of ‘picky’ mate selection.

However, during the dispersal flight and colony foundation of termites and many other eusocial insects, the potential for partner selection may be minimal due to the chaotic nature of mating swarms, when individuals only have a few minutes to find a partner and create an incipient colony or die. My anthropomorphic self likes to see it as an extreme form of speed dating. This mating behavior implies that being too choosy in mate preference would be counter-selected, especially when predation pressure is high. However, some lines of evidence suggest that ‘high quality’ primary reproductives could experience improved mating success, survival traits, fertility, and ultimately colony foundation success. Hence, despite an overall absence of mate selection, there could still be passive evolutionary selection for alate size or quality.

In termites, two main opposing selective forces may drive the evolution of the overall alate body size during colony foundation events.

The first selective force, as outlined by Nalepa (2011), is inherent to the biology of termites. Both the king and queen are monogamous partners, and each contributes to the biparental care of their first cohort of offspring. However, as the first functional workers emerge, the brood care duties irreversibly shift to the workers, resulting in constant alloparental care as the queen and king lose their ability to provide care for their brood (Chouvenc and Su 2017). Nalepa argued that in incipient termite colonies, the rapid switch from biparental care of the first brood to alloparental care of subsequent brood has resulted in reduced selection for the accumulation of large metabolic reserves in imagoes. As evidence for this, queen and king fecundity is maintained despite a relatively small body size (when compared to their ancestral wood roaches). The directional reduction of body size in termite imagoes may, therefore, have allowed mature termite colonies to increasingly invest into the number of alates to optimize their dispersal success rate.

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Young Coptotermes formosanus colony, where the workers have already taken over parental care duties.

The second selective force is opposite to the first one, as the limited metabolic reserves of relatively small termite alates during colony foundation leaves little room for inefficiency. The quality of the first brood is important for colony foundation success and the initial input from the queen and king are critical to jump-start the colony and improve its long term success within a highly competitive environment. Such pressure might incentivize mature colonies to invest in high-quality alates with enough internal metabolic resources to successfully produce their first cohort of functional workers during the incipient colony phase.

In dispersal fight events, Coptotermes gestroi alates may rapidly be killed by a wide range of predators. In this video, Pheidole megacephala was able to capture most alates that landed on trees or on the ground, which show how luck can be an essential factor on alate survival, independently of the quality of individuals.

In my 2019 study, I was able to take advantage of large dispersal flight events of Coptotermes gestroi (Rhinotermitidae) with high intracolonial and intercolonial variability in size to test the actual role of alate body size in colony foundation success and growth within the first nine months after foundation. I was able to measure 79% colony foundation success (n = 175), and most colonies that failed to establish had relatively small males and females, suggesting that mated pairs with relatively large individuals had a higher chance of surviving the first few months. This data suggests that, although the rapid transition to alloparental care in incipient colonies might reduce the need for accumulation of substantial reserves in alates, the mated pair still requires a bare minimum of initial metabolic resources to initiate efficient colony foundation and provide biparental care. Also, a positive correlation between the initial king and queen weights and colony growth was found despite high colony growth variability. Both the king and the queen initial weights were relevant for colony growth when considered separately, confirming the importance of biparental care, but when combined, only explained 27% of the observed variability despite highly standardized rearing conditions.

This study confirmed that during colony foundation in laboratory conditions, the initial weight of C. gestroi females and males plays a role in colony foundation establishment and initial colony growth rates. However, such laboratory results need to be placed in the perspective of the harsh conditions of field dispersal flights, where the vast majority of alates die rapidly and founding conditions are highly heterogeneous and hazardous. Therefore, the importance of alate weight may be secondary to many other environmental factors and luck. As previously suggested (Hartke and Bear 2011), sexual selection for large alate body size in termites during and after dispersal flights may be extremely weak and secondary to a wide variety of other selective pressures.

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Alates of Coptotermes gestroi emerging from a tree trunk by the thousands and ready to fly out.

Mating flights in C. gestroi termites can comprise hundreds of thousands of alates, and the large number of alates produced may be more relevant to the final number of established incipient colonies than the marginal advantage that relatively large alates may have during colony foundation. Such a reproductive strategy primarily relies on “inundative” dispersal flights, which may also have reduced the importance of alate weights during colony foundation. The trajectory of the reproductive strategy of a given termite species may partially be reflected in the size of their imagoes, an investment into reproduction which reflects the life history of the species. Over evolutionary time, termite colonies have optimized this quality/quantity trade-off in alate production, which varies among species.

In the light of its remarkable invasive abilities and its high colony establishment rate in the laboratory, C. gestroi may be a termite species that is able to efficiently optimize such balanced investment and adapt to various environmental pressures during dispersal flights and colony foundation.

References

Chouvenc, T., & SU, N. Y. (2017). Irreversible transfer of brood care duties and insights into the burden of caregiving in incipient subterranean termite colonies. Ecological entomology, 42(6), 777-784.

Chouvenc, T. (2019). The relative importance of queen and king initial weights in termite colony foundation success. Insectes Sociaux, 1-8.

Hartke, T. R., & Baer, B. (2011). The mating biology of termites: a comparative review. Animal Behaviour, 82(5), 927-936.

Nalepa, C. A. (2011). Body size and termite evolution. Evolutionary Biology, 38(3), 243-257.

Behind-the-scenes of the Insectes Sociaux best paper 2018

A blog post highlighting the article that received the prize for the best paper published in Insectes Sociaux in 2018 by Paul J. Davison and Jeremy Field.

By Paul Davison and Jeremy Field

 

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Jeremy at a Lasioglossum malachurum nest site in Spain

Paul’s Ph.D. focussed on the unusually varied social biology of sweat bees, which include eusocial species, solitary species and also socially polymorphic species. In socially polymorphic sweat bees, some populations have eusocial nests with a queen and workers, while in other populations of the same species all nests are solitary. Solitary populations are always found at cooler latitudes and/or higher altitudes than eusocial populations. Likewise, obligate eusocial species, in which nests always have queens and workers, never occur at the coolest latitudes or higher altitudes alongside solitary species or populations. The main element of the Ph.D. involved performing a field transplant to explore how the environment influences behaviour in a socially polymorphic sweat bee (for the results, see Davison & Field (2018) Behavioral Ecology & Sociobiology 72:56).

 

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A Lasioglossum malachurum foundress resting by the entrance to her new nest in spring

 

We thus became interested in what limits the geographic distribution of eusociality in sweat bees. It has long been thought that once the growing season becomes too short, it is no longer possible to sequentially produce the successive worker and reproductive broods necessary for eusociality and the only option is solitary nesting. Noticing that this had not been tested experimentally, we thought it would be interesting to do just that. The best way would be to conduct another transplant, only this time of an obligate eusocial sweat bee far to the north of its natural range.

 

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Freshly removed buckets containing newly dug nests ready to be packed for transplant

 

We chose to transplant Lasioglossum malachurum, a well-studied obligate eusocial sweat bee that is restricted to the south and east of Britain. We wanted to investigate the reasons for this, and in particular whether it is related to the length of the season. Because of other fieldwork commitments, this project would have to be ‘smash and grab’, or ‘smash and transplant’. Jeremy had the ingenious idea of getting spring foundresses to nest inside plastic buckets and then transplanting them and their nests wholesale. To do this, we spent winter digging trenches adjacent to where the bees nested in southern England, filling buckets with the excavated soil then putting them back into the trench and filling in the gaps. In essence, digging holes and filling them in again! By transplanting buckets after nests had been initiated in spring but crucially before foundresses began provisioning, we could test how being in a northern environment with a shorter season would impact the eusocial lifecycle.

 

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Embedding buckets in the garden of the University of Aberdeen’s Lighthouse Field Station at Cromarty (Photo: Paul Davison)

 

We were generously allowed to embed our transplanted buckets in the garden of the University of Aberdeen’s Lighthouse Field Station at Cromarty in northern Scotland. Cromarty is much further north than where L. malachurum occurs naturally and is a place most people have only heard of thanks to the BBC Radio 4 shipping forecast. Nestled between the 1840s lighthouse and stunning Cromarty Firth, the bees would certainly have a good view if nothing else. Equally generously, since it involves hours of scraping away at a block of soil on a table and is incredibly messy, Paul was able to excavate the buckets in rooms owned by the Cromarty Arts Trust. We transplanted control buckets to the University of Sussex campus, well within the bee’s natural range. All that remained was to see whether driving the length of Great Britain with buckets of nesting sweat bees would pay off.

 

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Digging a hole adjacent to the Lasioglossum malachurum nest aggregation in southern England for embedding buckets (Photo: Paul Davison)

 

The results were unequivocal. When we excavated the nests eight weeks after transplanting them, first brood offspring at Sussex were all nearing the completion of development, whereas in Scotland most offspring were still tiny larvae that had not long hatched. We estimated that this represented a lag of approximately seven weeks behind Sussex and that, had they been left to complete development, the first brood in Scotland would not have emerged as adults until August! This would leave no time for workers to provision a reproductive brood successfully. We found that the time lag corresponded to differences in temperature, which is well known to influence the timing of bee activity and seems to have caused foundresses in Scotland to begin provisioning much later in the spring. Importantly, this reflects environmental constraints on provisioning behaviour rather than the strategic shift between social and solitary nesting seen in some socially polymorphic sweat bees (Field et al. (2010) Current Biology 20:2028-31).

 

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A Lasioglossum malachurum nest entrance with a red marked female sitting just inside the entrance

 

All in all, some intriguing results. Jeremy is planning to take this initial work further with more replicates and a detailed study of what exactly causes the time lag.