Social parasitism: the keys to the kingdom

Highlighting the article by Leppänen, Seppä, Vepsäläinen and Savolainen in Insectes Sociaux

Written by Insectes Sociaux Editor in Chief, Michael Breed


Myrmica rubra. Photo credit: Tim Keppens/Flickr

How a species comes to exploit another species’ social advantages for survival is a rich and highly textured area of inquiry. Perhaps the most well known example of socially parasitic species are the slave-making ants, which steal the brood of other ant species and effectively make them ‘slaves’ working for the benefit of the slave-makers. Other types of social parasites exist only as queens, which live within the colony of a host species. How one species evolves to take advantage of another’s social system is an intriguing evolutionary question.

Intense discussion has focused on two very different models for how social parasites evolved. The first model proposes that social parasites evolve as sister species to their host. The social parasite is then initially similar to its host in communication and life history traits. This model is called Emery’s rule; the main difficulty with this route to social parasitism is that when it is strictly applied speciation occurs within a population, without geographic isolation.

It is easier to accept a relaxed interpretation of Emery’s rule, in which host and parasite are on the same very limited branch of a cladogram (evolutionary tree), but not necessarily sister species. Most supporting cases for Emery’s rule involve the relaxed interpretation, as it may not require speciation originating in the same geographical area. Genetic and morphological studies suggest that at least the relaxed version of Emery’s rule applies to many species of socially parasitic ants.

The second model invokes a common evolutionary ancestry, or clade that evolves with characteristics typical of certain kinds of social parasites, such as large size, a lack of foraging structures, a thick exoskeleton for protection against attack, and no worker caste. Members of this clade exploit other clades of the same general type of social insect. Species of the parasitic bee subgenus Psithyrus, which cladistically lies within the genus of their hosts, the bumblebees (Bombus), are good examples of this evolutionary model, as are members of the halictid bee subgenus Paralictus within Dialictus.

In this issue, Leppänen et al. (2016) present interesting data on mating isolation between macrogyne and microgyne populations of Myrmica rubra. The microgyne ants are workerless inquilines (social parasites) within the macrogyne colonies. Previous studies had suggested incomplete reproductive isolation between these sister populations of M. rubra.

However, it has been unclear how the mating system of Myrmica creates the opportunity for reproductive isolation between such sympatric populations of host and parasites. In a nicely designed set of genetic and mating compatibility tests, Leppänen and colleagues show that some ants prefer mate within their population, but that a small amount of cross-population gene flow likely occurs.

Leppänen et al. (2016) collected two kinds of data. First, they genotyped the gynes, worker, and males in colonies to determine the source of the males. In seven of the eleven nests studied, all males were produced by microgynes. In the remaining four colonies, males were produced either by macrogynes or by workers. Second, data on mating success of males were collected. Macrogyne (host) males mated more often with their own morphological type, whereas microgyne males seemed to succeed more evenly between the types/morphs.

The genetic differentiation between the two populations suggests speciation. Spatial separation of mating, with microgynes mating inside the nest and macrogynes mating in swarms, may explain the differentiation. The ability, however, of males to mate with either morphotype and the observation that microgyne males sometimes fly with swarms show that the evolutionary process that leads to mating isolation is incomplete in this system. To complete this story, a more thorough knowledge of the mating behavior of this species in the field will be required. Surprisingly little is known about the mating biology of many common species of ants, and gaining this knowledge will be difficult in examples like the microgynes of M. rubra, which mate within the nest.

Our understanding of the evolutionary processes that yield social parasites hinge on studies like this, which focus on species that are in an evolutionary dynamic state. Emery’s rule acknowledges that sister species have ‘‘the keys to the kingdom’’ in terms of shared communicatory mechanisms but the rule has a major weakness in requiring genetic isolation of sympatric populations.

Generally, the relaxation of Emery’s rule to incorporate species that have evolved in geographic isolation, and then come together, with one as host and the other as a parasite maintains the idea that commonality of social mechanism opens the door to parasitism, but that this can overlaid on a more plausible route to speciation. This study shows how genetic and behavioral data can be combined to help to shed light on these intriguing systems and that at least in some cases sympatric reproductive isolation should be considered as a mechanism.

Leppänen J, Seppä P, Vepsäläinen K, Savolainen R (2016) Mating isolation between the ant Myrmica rubra and its microgynous social parasite. Insect Soc 63:79–86. doi:10.1007/s00040-015- 0438-y

Interview with a social insect scientist: Patrizia d’Ettorre

Happy New Year social insect fans! I hope you enjoy this interview with Patrizia d’Ettorre. I definitely did.

IS:  Who are you and what do you do?

PD: I am an evolutionary biologist interested in the evolution of chemical communication and recognition of identity in social insects, mainly ants but also bees and wasps. I try to understand how they tell friends and enemies apart, how they make the difference between the smell of a queen and that of a worker and why some particular chemical compounds have been selected to play a significant role in communication. I am also interested in how ants perceive and process key chemical compounds.

 IS: How did you end up researching social insects?

PD: It was by chance. I wanted to study mammals, in particular Mustelidae, which are mostly solitary and nocturnal. However, at the end of my Master’s, I did an internship in the ant group of Professor Le Moli, at University of Parma, Italy and I became fascinated by these little social creatures.

 IS: What is your favourite social insect and why?

Polyergus Formica

Patrizia’s favourite ant, Polyergus rufescens (right) and its host, a Formica species (left).

PD: It the socially parasitic ant, Polyergus rufescens, the species I studied during my PhD. They are obligatory so-called ‘slave-makers’, meaning that they cannot live in absence of their host, which belongs to a different species of the genus Formica. The Polyergus queen is not able to found a new colony independently; she must enter a host nest and kill the resident queen. Therefore, the stock of host workers needs to be renewed. This is the job of the parasite workers, which go pillage the brood of neighbouring colonies of the host species. Being in the field and observing a Polyergus slave-raid is an impressive and amazing experience.

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

PD: There are several very nice moments, I am not sure I can say which was the best. One is when I discovered that Pachycondyla ant queens, which associate to found a new colony and aggressively establish dominance order, recognize each other individually. It was memorable since it was the last experiment I did myself, hands on, as a post doc. Another nice moment was when one of my post docs and a PhD student discovered the first ant queen pheromone regulating worker reproduction (in Lasius niger). However, since we always work ‘blind’, these great moments are typically coming at the end of the experiments, when we look at the graphs and do the statistics, which is usually not very poetic as a moment. A different kind of hurrah! moment was when one of my post-docs showed me the video of a harnessed Camponotus ant learning to associate an odour to a sugar reward. This was the establishment of the maxilla-labium extension response protocol, and we now can study perception, learning and memory in ants using a controlled procedure similar to the one used with honey bees.

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

 PD: Yes, I teach and I like teaching. I teach principally human ethology, cognitive ethology and ontogeny of behaviour. Yes, I use examples from social insects in my teaching, even in human ethology when I talk about collective behaviour.

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

PD: I am reading “Darm mit Charme” by Giulia Enders (the French version). It is a journey along our digestive system; it is instructive, funny and nicely illustrated. I would recommend it because it is an entertaining way to know something new about our body and it is a vey nice example of science communication to the general public.

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

PD: I was a young teenager when I read “King Solomon’s Ring” by Konrad Lorenz, and I loved it. This book probably influenced my choice of studying animal behavior.

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

PD: Outside science? Is there anything? 🙂
I like cooking for my friends, going to a nice restaurant, going for a walk in a park with my dogs, going to the cinema, concerts, and so on. Recently, I developed an interest for rugby, it took me a while to understand the rules though.

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

PD: A little chocolate now and then.

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

PD: Two are not really ‘things’ but they are my two dogs, Livio and Gioia. I would bring them because they are fun. Then, I would probably bring a towel, you should never travel without a towel.

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

PD: This is a difficult question. I had several excellent mentors. They all had a great influence on my career, and at different stages, from Master’s student to senior post doc. I became a truly independent researcher in Koos Boomsma’s lab. I believe Koos contributed significantly to my intellectual independence. My students have a substantial influence on the direction I will take next; I had the most inspiring and enjoyable discussions with Jelle van Zweden, Volker Nehring and Nick Bos when they were PhD students.

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

 PD: Be passionate, be enthusiastic, be reliable, be rigorous, be curious … and be stubborn.