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
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Author for correspondence:
Javier Hernandez Lopez
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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)