In late September, as the UK was enjoying the last vestiges of summer I was lucky enough to head to Orlando in Florida where the 25th International Congress of Entomology was being held under the banner of “Entomology without borders”. This year, Orlando welcomed over 7000 delegates working in all areas of entomology; the largest gathering of entomologists at any one time – as far as we know! I first attended this enormous event, held every 4 years, as a young PhD student in 2000, in the beautiful city of Iguassu Falls in southern Brazil. I have been able to attend 3 of the 4 subsequent meetings, and co-hosted a session on Ecological immunology of Insects in each one, first in Brisbane, Australia (2004), then in Durban, South Africa (2008), and finally in Orlando. Much as I would like to have a clean sweep, maternity leave put paid to my plans to attend the 2012 meeting in Seoul, South Korea.
Ecological immunology aims to understand how ecological pressures have shaped the evolution and expression of the immune system. In 2000, this was a very new concept that was just gaining ground in the ecological literature. Over the last 16 years this has grown into an established field. A quick search on Web of Science for the terms “Ecological immunology” or “Eco-immunology” shows a steady increase in publications over time. Of course, this does not find all of the papers in the field of eco-immunology, just those that specifically use that term, but it is indicative of how the field has rapidly grown.
Of those who work in eco-immunology, while there are significant bodies of work on birds and rodents, many have chosen to focus on insects as model systems. The ease with which they can reared in the lab in great numbers makes them ideal to ask questions about how immune investment under different ecological conditions affects fitness. This rapid growth of interest was reflected in the symposia on offer in Orlando. There was a wealth of research in insect immunology, with 12 symposia on this theme, ranging from the heavily mechanistic, “Biochemical signalling interface between invaders and their insect hosts” to the eco-focussed “Trade-offs and immunity: Physiology, Life-History and Evolution” and my own symposium, “Eco-Immunology of Invertebrates”. There were excellent talks from many international speakers, ranging from graduate students to established Professors; here I highlight some of my favourites.
Erica Harris, working in Nicole Gerardo’s lab at Emory in the US, was the well-deserved winner of the prize for the best graduate talk in immunology. Her engaging talk was the first to pick up on the theme of how gut microbiota can modulate immune responses, a topic that will also be highlighted in the forthcoming JAE special issue on animal-microbe interactions. Working with Monarch butterflies (Danaeus plexippus), their larval food plants (Asclepias spp.), and protozoan parasites (Ophryocystis elektroscirrha), Erica’s work has focussed on assessing how host diet affects gut bacterial communities and how differences in these communities could explain host-parasite interactions on different host plants.
Nichole Broderick, an Assistant Professor at the University of Connecticut, expanded this theme by asking the question, “Did the immune system arise due to interactions between the gut and microbes in terms of feeding and digestion?” Arguments for include the dual use of immune molecules, such as lysozyme and phenoloxidases, in digestion and immunity. Drosophila, her model organism, eats yeasts and bacteria on rotting fruit. Nichole found that in immune-deficient flies, there was an increased density, diversity and distribution of bacteria in the gut compared to Wild-type flies, whose bacteria were localised in the hind midgut. Interestingly, immune-deficient flies showed dysregulation of immune and metabolism genes in response to microbiota, and showed delayed development and reduced fecundity, indicative of metabolic defects, highlighting the link between immunity to, and digestion of, microbes.
Paul Johnston, a postdoctoral researcher in Jens Rolff’s lab in the Frei Universitat Berlin then asked “What happens to gut microbiota during complete metamorphosis in insects?” This is a period of complete reorganisation of the insect body and to date the assumption has been that gut microbiota are lost during this time either by defecation, or by sterilisation of the gut prior to its breakdown (amusingly described as the “death-turd hypothesis”). In contrast, Paul’s experiments have shown that the host and their microbiota work together to ensure survival of the microbiota during metamorphosis and that disruption of either partner alters the microbial composition, leading to serious fitness costs.
Insects using pathogens to prime themselves, their nestmates or their offspring against future infections was another key theme of the talks. Barbara Milutinovic, a postdoctoral researcher with Sylvia Cremer at IST in Austria, looked at how socially acquired, low dose Metarhizium fungal infections, improved an ant’s resistance to the fungus in future infections. Priming across generations was discussed in multiple taxa. Ben Sadd, an Assistant Professor at Illinois State University, looked at costs of immune priming in bumblebees, showing that bees transgenerationally primed with bacteria were more susceptible to a trypanosome infection in the gut. Yannick Moret, Director of Research CNRS at the University of Bourgogne, examined the specificity of immune priming by comparing responses of mealworm beetles, Tenebrio molitor, and their offspring to priming with gram positive or negative bacteria. Priming with gram positive bacteria was protective against Gram positive and negative pathogens, as it induced a persistent antibacterial response, which did not occur with gram negative priming. For the offspring, however, the bacteria their mothers were primed with did not affect the level of protection they received.
Charlotte Miller, my own PhD student, showed that burying beetles, Nicrophorus vespilloides, were more likely to survive a bacterial infection if their mothers had been primed with a live pathogen, but not with an immune elicitor. Moreover, offspring from primed mothers showed an improved social immune response, the antibacterial exudate they produce for the benefit of their offspring, suggesting that priming beetles can benefit their grandchildren! Dalial Freitak, a researcher at the University of Helsinki, addressed a potential mechanism behind this priming across generations. She demonstrated that, in honeybees, vitellogenin, a vital protein component of eggs, is able to bind bacterial fragments and take them into eggs, thus vaccinating the offspring against disease.
Finally, an excellent and thought-provoking talk by Paul Schmid-Hempel, Professor at ETH Zurich, called for more of us to take our immunology into the field, to considerably enhance the “eco” in eco-immunology. I’m looking forward to the 26th ICE in Helsinki, Finland, in 2020 to see how many people have heeded Paul’s advice!