Trans-generational immune priming in honeybees

Proceedings of the Royal Society B: Biological Sciences, Jun 2014

Maternal immune experience acquired during pathogen exposure and passed on to progeny to enhance resistance to infection is called trans-generational immune priming (TgIP). In eusocial insects like honeybees, TgIP would result in a significant improvement of health at individual and colony level. Demonstrated in invertebrates other than honeybees, TgIP has not yet been fully elucidated in terms of intensity and molecular mechanisms underlying this response. Here, we immune-stimulated honeybee queens with Paenibacillus larvae (Pl), a spore-forming bacterium causing American Foulbrood, the most deadly bee brood disease worldwide. Subsequently, offspring of stimulated queens were exposed to spores of Pl and mortality rates were measured to evaluate maternal transfer of immunity. Our data substantiate the existence of TgIP effects in honeybees by direct evaluation of offspring resistance to bacterial infection. A further aspect of this study was to investigate a potential correlation between immune priming responses and prohaemocytes–haemocyte differentiation processes in larvae. The results point out that a priming effect triggers differentiation of prohaemocytes to haemocytes. However, the mechanisms underlying TgIP responses are still elusive and require future investigation.

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Trans-generational immune priming in honeybees

Javier Hernndez Lpez 0 Wolfgang Schuehly 0 Karl Crailsheim 0 Ulrike Riessberger-Gall 0 0 Department of Zoology, Karl-Franzens University of Graz , Universita tsplatz 2, 8010 Graz , Austria Articles on similar topics can be found in the following collections Receive free email alerts when new articles cite this article - sign up in the box at the top right-hand corner of the article or click here References Subject collections Email alerting service rspb.royalsocietypublishing.org Research Author for correspondence: Javier Hernandez Lopez e-mail: Electronic supplementary material is available at http://dx.doi.org/10.1098/rspb.2014.0454 or via http://rspb.royalsocietypublishing.org. Trans-generational immune priming in honeybees Javier Hernandez Lopez, Wolfgang Schuehly, Karl Crailsheim and Ulrike Riessberger-Galle Maternal immune experience acquired during pathogen exposure and passed on to progeny to enhance resistance to infection is called trans-generational immune priming (TgIP). In eusocial insects like honeybees, TgIP would result in a significant improvement of health at individual and colony level. Demonstrated in invertebrates other than honeybees, TgIP has not yet been fully elucidated in terms of intensity and molecular mechanisms underlying this response. Here, we immune-stimulated honeybee queens with Paenibacillus larvae (Pl), a spore-forming bacterium causing American Foulbrood, the most deadly bee brood disease worldwide. Subsequently, offspring of stimulated queens were exposed to spores of Pl and mortality rates were measured to evaluate maternal transfer of immunity. Our data substantiate the existence of TgIP effects in honeybees by direct evaluation of offspring resistance to bacterial infection. A further aspect of this study was to investigate a potential correlation between immune priming responses and prohaemocytes haemocyte differentiation processes in larvae. The results point out that a priming effect triggers differentiation of prohaemocytes to haemocytes. However, the mechanisms underlying TgIP responses are still elusive and require future investigation. 1. Introduction Recent studies involving different species of insects have expanded the knowledge of immunology in invertebrates, but also increased the understanding of its limits [1 7]. Invertebrates were previously believed to rely purely on their innate defences to combat infections [8], and specificity or memory of immune responses were previously considered the hallmark of a highly evolved immune system, only present in vertebrates. Research, however, has revealed that the immune system of invertebrates shares several homologies with that of vertebrates [9 12]. Although the invertebrate immune system lacks lymphocytes and functional immunoglobulins, an increasing number of studies cite induced immune responses in invertebrates which in some cases indicate specificity [13,14]. Other studies have identified haemocytes to be responsible for the specificity of these responses. Cumulatively, these studies show that encounters with a pathogen can enhance the phagocytic activity of haemocytes and mediate specificity in immune protection [15 18]. Moreover, maternal immune experience has been demonstrated to be transmitted to progeny and may therefore have a positive impact on offspring resistance and survival of infections. This phenomenon of trans-generational immune priming (TgIP) has been reported in both vertebrates [19,20] and invertebrates [21 27]. Nevertheless, the magnitude of this response and the underlying molecular mechanisms are still poorly understood in invertebrates. Honeybees are social insects, forming colonies composed of up to 50 000 individuals or more, residing in a minimal space that offers ideal conditions for the transmission of pathogens and parasites [28]. They show high levels of sociability and physical contact between individuals and environmental homeostasis inside the colony is highly controlled. Offspring are likely to face the same pathogen pressures as queens and could benefit from TgIP effects. In such an environment, the mother queen, upon immunological encounter with a pathogen, could & 2014 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original author and source are credited. cumulative mortality at day 12 (number of larvae and replicates per colony) pre-challenge (%) nucleus colonies full colonies nucleus colonies influence the immunity of direct progeny, thus increasing resistance to current infection in the colony. Here, we investigated the occurrence of TgIP in honeybees by immune-challenging queens with heat-killed bacteria of Paenibacillus larvae (Pl), causative agent of American foulbrood (AFB) [29] and exposing their first instar larvae to Pl spores. AFB is considered to be the most threatening bacterial disease of honey (...truncated)


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Javier Hernández López, Wolfgang Schuehly, Karl Crailsheim, Ulrike Riessberger-Gallé. Trans-generational immune priming in honeybees, Proceedings of the Royal Society B: Biological Sciences, 2014, 281/1785, DOI: 10.1098/rspb.2014.0454