Induced immune responses in Formica fusca

In the recently published paper “Induced immune responses in Formica fusca (Hymenoptera: Formicidae)”, Siiri Fuchs, Liselotte Sundström, Nick Bos, Dimitri Stucki, and Dalial Freitak stimulated the immune system of F. fusca queens with dead conidia of the fungus Beauveria bassiana and checked for changes in the expression of immunity-related genes. They revealed that larvae produced by untreated queens had a higher mortality compared with larvae produced by immune-primed queens. Also immune-gene expression levels showed changes, both in queens and their offspring. Here, Simon Tragust highlights their main points.

A Review compiled by Simon Tragust

In a recent paper in Myrmecological News, Siiri Fuchs and co-authors set out to investigate the presence of immune memory in the ant Formica fusca. Immune memory can loosely be described as enhanced protection after re-exposure to a pathogen and was long thought to be a unique hallmark of the vertebrate adaptive immune system. Over the last 20 years, however, an increasing number of studies indicated the existence of memory-like immune responses in invertebrates (Contreras-Garduno & al. 2016, Milutinovic & Kurtz 2016). These memory-like responses, often termed immune priming, can provide protection for either the individual (within-generational priming) or its offspring (transgenerational priming). Although studies on immune priming in invertebrates vary considerably in their experimental design, the principal approach is often the same. Investigations either use a low dose of a pathogen that does not lead to any obvious infection or inactivated pathogens to prime individuals and then, after a time-delay, use a high dose or a living pathogen to challenge the individual or its offspring (Little & Kraaijeveld 2004). Enhanced immune response, parasite clearance, and/or host survival compared with unchallenged individuals are then interpreted as evidence of a memory-like response.

Formica fusca queen with the worker. (© Liselotte Sundström)

In social Hymenoptera, immune priming has been shown in bumblebees (Sadd & al. 2005, Sadd & Schmid-Hempel 2006, 2009) and honey bees (Hernandez Lopez & al. 2014) with transgenerational immune priming occurring via elicitors in the eggs (Sadd & Schmid-Hempel 2007, Salmela & al. 2015). Across ants, evidence for immune priming is much more contradictory. No evidence for immune priming with a fungal entomopathogen was found in workers of Formica selysi (Reber & Chapuisat 2012), while priming was found in larvae of Camponotus pennsylvanicus with a bacterial pathogen (Rosengaus & al. 2013). Priming is also found in workers of Lasius neglectus for a fungal entomopathogen (Ugelvig & Cremer 2007, Konrad & al. 2012) but depends on the type of fungal pathogen used (Konrad & al. 2018). Transgenerational immune priming has not been assessed in ants so far. In their recent paper “Induced immune responses in Formica fusca (Hymenoptera: Formicidae)” Siiri Fuchs and co-authors finally set out to fill this gap. They found that larvae and workers of queens primed with a fungal entomopathogen through injection did not survive a subsequent challenge significantly better compared with offspring of control-primed queens. Also, they found that some of the nine immune genes investigated were upregulated in fungus-primed queens but downregulated in their larvae compared with larvae from control-primed queens.

This absence of transgenerational immune priming in ants appears surprising, especially given the following evidence: Firstly, within-generation priming was not found in queens of Formica selysi but in queens of Lasius niger, in the latter species only with mated but not virgin queens (Galvez & Chapuisat 2014). Secondly, pathogen-induced network changes within Lasius niger colonies can increase the probability of queens receiving a sub-lethal pathogen challenge, thus potentially promoting transgenerational immune priming (Stroeymeyt & al. 2018). Thirdly, ant queens of Formica selysi are attracted to fungal pathogens during colony foundation, which might be beneficial under transgenerational immune priming (Brütsch & al. 2014). Finally, most ant queens and ant colonies are arguably long-lived, and transgenerational immune priming has been suggested to be more likely to have evolved in long-lived species (Little & Kraaijeveld 2004, Pigeault & al. 2016). Since immune priming in ants apparently depends on many factors, the study by Siiri Fuchs and co-authors highlights the need to establish the evolutionary and ecological factors under which immune priming manifests in ants. In my view, an opportunity to grasp.

Dalial Freitak collecting Formica fusca colonies from Tvärminne area for experiments. (© Dalial Freitak)

References

Brütsch, T., Felden, A., Reber, A. & Chapuisat, M. 2014: Ant queens (Hymenoptera: Formicidae) are attracted to fungal pathogens during the initial stage of colony founding. – Myrmecological News 20: 71-76.

Contreras-Garduno, J., Lanz-Mendoza, H., Franco, B., Nava, A., Pedraza-Reyes, M. & Canales-Lazcano, J. 2016: Insect immune priming: ecology and experimental evidences. – Ecological Entomology 41: 351-366.

Galvez, D. & Chapuisat, M. 2014: Immune priming and pathogen resistance in ant queens. – Ecology and Evolution 4: 1761-1767.

Hernandez Lopez, J., Schuehly, W., Crailsheim, K. & Riessberger-Galle, U. 2014: Trans-generational immune priming in honeybees. – Proceedings of the Royal Society B-Biological Sciences 281: art. 20140454.

Konrad, M., Pull, C.D., Metzler, S., Seif, K., Naderlinger, E., Grasse, A.V. & Cremer, S. 2018: Ants avoid superinfections by performing risk-adjusted sanitary care. – Proceedings of the National Academy of Sciences of the United States of America 115: 2782-2787.

Konrad, M., Vyleta, M.L., Theis, F.J., Stock, M., Tragust, S., Klatt, M., Drescher, V., Marr, C., Ugelvig, L.V. & Cremer, S. 2012: Social transfer of pathogenic fungus promotes active immunisation in ant colonies. – Public Library of Science Biology 10: art. e1001300.

Little, T.J. & Kraaijeveld, A.R. 2004: Ecological and evolutionary implications of immunological priming in invertebrates. – Trends in Ecology & Evolution 19: 58-60.

Milutinovic, B. & Kurtz, J. 2016: Immune memory in invertebrates. – Seminars in Immunology 28: 328-342.

Pigeault, R., Garnier, R., Rivero, A. & Gandon, S. 2016: Evolution of transgenerational immunity in invertebrates. – Proceedings of the Royal Society B-Biological Sciences 283: art. 20161136.

Reber, A. & Chapuisat, M. 2012: No evidence for immune priming in ants exposed to a fungal pathogen. – Public Library of Science One 7: art. e35372.

Rosengaus, R.B., Malak, T. & Mackintosh, C. 2013: Immune-priming in ant larvae: social immunity does not undermine individual immunity. – Biology Letters 9: art. 20130563.

Sadd, B.M., Kleinlogel, Y., Schmid-Hempel, R. & Schmid-Hempel, P. 2005: Trans-generational immune priming in a social insect. – Biology Letters 1: 386-388.

Sadd, B.M. & Schmid-Hempel, P. 2006: Insect immunity shows specificity in protection upon secondary pathogen exposure. – Current Biology 16: 1206-1210.

Sadd, B.M. & Schmid-Hempel, P. 2007: Facultative but persistent trans-generational immunity via the mother’s eggs in bumblebees. – Current Biology 17: R1046-1047.

Sadd, B.M. & Schmid-Hempel, P. 2009: A distinct infection cost associated with trans-generational priming of antibacterial immunity in bumble-bees. – Biology Letters 5: 798-801.

Salmela, H., Amdam, G.V. & Freitak, D. 2015: Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin. – Public Library of Science Pathogens 11: art. e1005015.

Stroeymeyt, N., Grasse, A.V., Crespi, A., Mersch, D.P., Cremer, S. & Keller, L. 2018: Social network plasticity decreases disease transmission in a eusocial insect. – Science 362: 941-945.

Ugelvig, L.V. & Cremer, S. 2007: Social prophylaxis: group interaction promotes collective immunity in ant colonies. – Current Biology 17: 1967-1971.

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