Ready to rebel to an almost royal queen: brain genes and social networks unveil the hidden side of a coevolutionary arms race in Polistes wasps

By Alessandro Cini

A blog post accompanying the Best Paper Announcement for 2020, just out online in Insectes Sociaux. And while you’re at it, why not (re)read Alessandro Cini, Rebecca Branconi, Solenn Patalano, Rita Cervo, and Seirian Sumner ‘Behavioural and neurogenomic responses of host workers to social parasite invasion in a social insect‘, Insectes Sociaux 67, pages 295–308 (2020)!

Social insect colonies represent meaty resources for parasites and predators, but even more so for obligate social parasites, i.e. those species which have evolved to exploit on what is probably the most precious resource within the colony of social insects: alloparental brood care. The exploitation of this energy-expensive social trait is so rewarding that indeed several species of ants, bees and wasps have even lost some of their defining traits as social insects, i.e. nest building and production of the worker caste, thus becoming completely dependent on the host species.

The huge selective pressure to defeat the host species equipped these obligate social parasites with a plentiful bouquet of adaptations, from enlarged and thickened body parts, to better engage in violent fights, to sophisticated sensory tricks, to break the host communication code and deceive its social system. These adaptations are so astonishing that we often forget that there is indeed another player in the game: the host! Hosts as well are under strong selection pressure to put in place effective defensive strategies and prevent, or at least reduce, the fitness costs imposed by the presence of the social parasite. Indeed, even after a successful colony takeover, even if the social parasite might look utterly integrated, its throne possession should not be taken for granted.

Two main types of “last-resort” host reactions have been so far identified. First, host workers openly react to the social parasite, as it happens in Temnothorax ants, by identifying the offspring of the parasite and killing it. Otherwise, the reaction can be more concealed. This is the case of the paper wasp Polistes dominula, the unique host species of the obligate inquiline social parasite Polistes sulcifer (figure 1). Here, rather than directly facing the parasite or its offspring, the workers adopt a subtle strategy which sees them working for the parasite while at the same time investing in their own reproduction. Indeed, as I found together with colleagues from University of Florence and University Pierre et Marie Curie some years ago, host workers perceive that something is going wrong in their colony and react by developing ovaries. This physiological reaction makes them “ready to go” for their own direct fitness, meaning that they are ready to lay eggs if the opportunity arises. Thus, the parasitic female queen is indeed, as we called it at that time, “Almost royal”.

Figure 1. The socially parasitic queen of Polistes sulcifer has usurped the colony since a few days, and she stands, apparently quiet, in the middle of the comb…Is she aware that the host workers are “plotting” against her royalty?!

This discovery represented an exciting moment of my PhD, as we were somehow dismantling the stereotype of the super-powerful and neatly integrated social parasite. But clearly, this evidence raised a wealth of questions on both the ultimate and proximal reasons of this interaction:  is it the lack of suppression of worker reproduction by the social parasite reflecting its inability to control host worker reproduction or is it rather a concession to workers (a sort of incentive to stay and help)? Also, which were the cues on which workers detected the change in the “throne” ownership?

Understanding the timing of the worker reaction is crucial to start answering these questions, as the costs and benefits for both parties depend on when the workers start rebelling.  However, while our first study demonstrated that a reaction was already in place in the long term (at least five-six weeks after the colony takeover), it did not clarify when it started.

We thus combined two tools, brain transcriptomics and analysis of social networks, to look for potential early markers of such an intriguing rebellion. As it usually happens, we took great advantage of some useful prior knowledge. First, we (especially thanks to the smart expertise of Solenn Patalano, at that time post-doc in London) looked at some candidate genes supposedly changing between reproductive and non-reproductive wasps. We predicted that if workers were reproductively rebelling to the social parasite, their genetic expression should have switched from a “non-reproductive”-like gene expression pattern to a more “reproductive”-like one. Indeed, we detected that soon after the usurpation (within the first two weeks from the colony takeover) one gene, the Imaginal disc growth factor (Idgf4) gene, considered to be responsive to changes in the social environment, was significantly down-regulated in workers from parasitized colonies. This might suggest that parasitized workers are anticipating a shift toward a less worker-like phenotype in preparation for their reproductive rebellion.

Then we (actually the passionate and meticulous Rebecca Branconi, at that time Master student in Florence) analysed several hours of video recordings to understand the fine-scale dominance behaviour of workers, knowing that in P. dominula societies the dominant and reproductive individuals are the most central ones in the colonial social network. Here again, we found a clear signature of a shift in individual centrality for parasitized workers already two weeks after the usurpation. As expected, where the parasite replaced the host queen, workers changed their social behaviour, performing and receiving more dominance acts, in a sort of potential fine-level social reorganization of the colony. Thus, both gene expression and social network analyses concurred in suggesting that workers were rapidly reacting to the parasite presence, well before any physiological change was evident.

In the coevolutionary arms race between the social parasite and the host, thus, host workers might be more ahead than we have been thinking. While this arms race has been running for a long time, we are just now uncovering some if its most fascinating sides.  

This Insectes Sociaux prize for the best paper is extremely welcome! First, as it comes from the reference journal of our community, a community in which I grew up scientifically thanks to many people and many shared scientific moments. Second, as it rewards a collective effort made with people whose expertise and knowledge enriched and thrilled me over these years, and in particular two amazing and inspirational mentors, Rita Cervo and Seirian Sumner, which I thus heartily thank!  

Some references to deepen the topic

Achenbach, A., & Foitzik, S. (2009). First evidence for slave rebellion: enslaved ant workers systematically kill the brood of their social parasite Protomognathus americanus. Evolution: International Journal of Organic Evolution63(4), 1068-1075.

Grüter, C., Jongepier, E., & Foitzik, S. (2018). Insect societies fight back: the evolution of defensive traits against social parasites. Philosophical Transactions of the Royal Society B: Biological Sciences373(1751), 20170200.

Cini, A., Sumner, S., & Cervo, R. (2019). Inquiline social parasites as tools to unlock the secrets of insect sociality. Philosophical Transactions of the Royal Society B374(1769), 20180193.

Cini, A., Nieri, R., Dapporto, L., Monnin, T., & Cervo, R. (2014). Almost royal: incomplete suppression of host worker ovarian development by a social parasite wasp. Behavioral ecology and sociobiology68(3), 467-475.

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