Avian maternal transfer of antibodies: are they affecting the specific immune response of their chicks?
Author(s): Broggi, J, Soriguer, RC, Figuerola, J
Avian parents influence their offspring’s phenotypes by providing different sorts of parental care. Mothers may transfer a variety of elements through the yolk sack that can affect the embryo’s development. Among these elements supplied, mothers transfer antibodies that provide transient adaptive immune protection to the chick. However, whether such transient specific immunity is enhancing the chicks’ subsequent immune response to the same specific immune challenge remains controversial. We explored whether mother’s specific immune response to Newcastle disease virus (NDV) affected their chick’s subsequent response to the same antigen. We studied a wild breeding population of house sparrow (Passer domesticus) in southern Spain. We captured 57 breeding females in two consecutive breeding events: 29 were vaccinated against NDV in their first brood, and the rest were sham-controlled. Chicks on their second brood were equally treated, the concentration of NDV antibodies (NDV-Ab) was measured, and the phytohaemaggulutinin-induced immune response (PHA) assayed from all before fledging. Leukocyte profile, antioxidative status and total protein concentration from blood was measured from all individuals. Both vaccinated mothers and chicks presented higher NDV-Ab levels than control individuals. Chicks’s level of NDV-Ab was marginally affected by their mother’s treatment, which was further confirmed when the level of maternal NDV-Ab was taken into consideration. Chicks challenged with NDV vaccine developed a stronger specific response whenever their mothers presented high levels of NDV-Ab. However, chick’s PHA response was unaffected by none of the treatments, nor the mothers’ condition (NDV-Ab, leukocyte profiles or antioxidative status) in any way. Our results suggest that house sparrow mothers transfer specific NDV-Ab, which help their chicks to respond more strongly when challenged with the same antigen, leaving other immune responses unaffected.
Institute of Evolutionary Biology
Changes in feeding rate can explain the maternal effect of food on disease resistance in Daphnia magna
Author(s): Garbutt, JS, Wilson, PJ, Little, TJ
Maternal effects are increasingly recognised to impact on infectious disease. In invertebrates, maternal parasite exposure, as well as changes in maternal abiotic environment (e.g. food availability, crowding, forced-flight), have been shown to influence the outcome of offspring-parasite interactions with profound fitness consequences for the host. An understanding of the mechanisms underlying these maternal effects is a prerequisite for recognising their adaptive value, yet proximate mechanisms have so far received little attention. We investigated the mechanism underlying a maternal effect on disease resistance in the crustacean Daphnia magna, an organism that produces offspring more resistant to the sterilising bacterium Pasteuria ramosa when food availability is relatively poor. We show that this maternal effect is likely to be mediated by a reduction in feeding rate in the offspring of food stressed mothers, explaining their improved resistance to a parasite that infects via the gut.
Department of Ecology and Evolution
Foster care-givers influence brood pathogen resistance in ants
Author(s): Purcell, J, Chapuisat, M
Social organisms face a high risk of epidemics, and respond to this threat by combining efficient individual and collective defenses against pathogens. An intriguing and little studied feature of social animals is that individual pathogen resistance may depend not only on genetic or maternal factors, but also on the social environment during development. Here, we used a cross-fostering experiment to investigate whether the pathogen resistance of individual ant workers was influenced by their care-givers’ or their own colony of origin. The ability of newly eclosed, cross-fostered Formica selysi workers to resist the fungal entomopathogen Beauveria bassiana was influenced by the workers that cared for them during development. This effect persisted even in the absence of ongoing social interactions and did not depend upon the social structure of the colony of origin of either care-givers or brood. Social interactions during development thus influence individual resistance, blurring the line between individual and social immunity.
School of Biological and Chemical Sciences
Maternal investment and larval fitness in the burying beetle Nicrophorus vespilloides
Author(s): Littlefair, J, Arce, A, Rozen, D, Knell, R
Studies of transgenerational immune priming have shown that an immune challenge to parents can lead to upregulated offspring immunity and increased resistance to disease1,2. Here we investigate whether mothers can anticipate immune challenges to their offspring by assessing the quality of resources that will be available to offspring. When resources are spatially and temporally variable, it could be adaptive to alter the offspring phenotype accordingly.
The burying beetle Nicrophorus vespilloides feeds and reproduces on carrion. Females will breed multiple times during their lives, and carcasses will vary in levels of decomposition throughout their lifespan. Their offspring will therefore experience different levels of competition and challenges from micro-organisms, as well as variation in nutritional quality. Parents examine and carefully prepare carcasses for their broods, giving mothers an opportunity to assess the quality of the reproductive resource during this preparation phase.
We tested the hypothesis that beetle mothers can anticipate the offspring’s environment during the preparation of the resource and match offspring phenotype to this by adjusting immune investment and/or development. We performed a cross-factorial experiment in which mothers bred on resources of either good or poor quality, and newly hatched larvae were transferred onto resources of either the same or different quality. During their final larval instar, traits relating to fitness and immune defence were measured. Adult life history traits from the offspring generation were also assessed, and we present those findings here.
1 Tidbury, H., Pedersen, A., Boots, M. 2011 Within and transgenerational immune priming in an insect to a DNA virus Proc. R. Soc. B 278, 871-876 2 Sadd, B.M., Kleinlogel, Y., Schmid-Hempel, R. & Schmid- Hempel, P. 2005 Trans-generational immune priming in a social insect. Biol. Lett 1, 386–388
Institute for Evolution and Biodiversity
Oral immune priming in the red flour beetle Tribolium castaneum
Author(s): Milutinovic, B, Fritzlar, S, Kurtz, J
The phenomenon of immune priming and its transfer to the offspring as trans-generational priming has now been demonstrated for number of insect species, including the red flour beetle Tribolium castaneum. For testing this phenomenon, the majority of studies have focused on introducing the pathogen into the insects' hemolymph by making a small wound in the cuticle. Although such septic injury can occur in nature, many pathogens are able to infect their hosts also via the oral route, i.e. by uptake with the food. Bacillus thuringiensis is a spore-forming, entomopathogenic bacterium, which infects its hosts in this way, and penetrates the host gut epithelium to gain access to the hemocoel. We tested for immune priming of T. castaneum larvae by oral exposure to B. thuringiensis vegetative cells and spores, as well as by media supernatants from bacterial cultures. We found strong induction of immune priming when we exposed the larvae to the sterile media in which bacteria were raised, but not to the heat-killed bacteria, killed spores or low amounts of viable spores. Primed larvae showed increased survival upon oral challenge with a high dose of B. thuringiensis spores. Moreover, they had a longer developmental time, indicating that investment in such a priming response comes with a cost. We moreover show that increased survival in larvae exposed to the priming-inducing diet was not caused by a difference in the size of larvae after priming. We are currently testing for trans-generational oral priming, i.e. whether the offspring of primed individuals shows increased survival upon challenge.
Priming against pathogen attack in Caenorhabditis elegans – effect of probiotics or immune system activation?
Author(s): Schulte, RD, Hanke-Uhe, M, Kubela, A
Parasites impose strong selective pressures on hosts since they reduce per definition host fitness. Immune reactions are advantageous, but they are also costly. Therefore, mechanisms reducing the costs of a continuous expression of immune genes are selected. An alternative strategy is the behavioural defence, for example escape behaviour. Hosts prevent contact to parasites by escaping potentially dangerous areas, particles or individuals. For the nematode Caenorhabditis elegans such escape behaviour is well known: It escapes pathogenic bacteria and prefers feeding on non-pathogenic variants of the same bacterial species. We here ask whether feeding on these non-pathogenic bacterial variants offers another advantage than just the uptake of non-pathogenic food. In detail we test whether previous contact to non-pathogenic Bacillus thuringiensis is advantageous upon later contact to pathogenic B. thuringiensis. We found indeed that nematodes with previous contact to the non-pathogenic bacteria survive better upon contact to pathogenic bacteria. Since this effect is equally strong if the non-pathogenic bacteria are alive or dead, this effect is most likely caused by an immune activation and not by the probiotic accumulation of non-pathogenic bacteria in the gut. These results highlight that also in species with a primitive immune system immune priming may occur, also the exact mechanism remains unclear.
Department of Zoology and Physical Anthropology
The role of maternal effects on the ontogeny of constitutive immunity in wild birds
Author(s): Arriero, E, Martin, TE
The ability to resist infections early in life is expected to be under intense selection pressure because infection may have severe impact on fitness. Maternally transmitted immune components provide some protection during early stages and may have long-lasting effects on the development of the humoral immune system. Extrinsic influences on mothers (i.e. exposure to pathogens) may also influence vertical transmission of immune components to offspring. However, maternal effects on the ontogeny of offspring immune function may not be restricted to vertically transmitted components. Mothers may influence the development of offspring immune function by providing a suitable environment for embryo development through parental care. Indeed, parental behaviour in birds plays an important role in keeping embryo thermal conditions within the optimal range for development. This parentally induced variation in embryo temperatures can thereby influence development and performance of the immune system. Yet, whether these maternal effects mediated by egg constituents or thermal environment interact with endogenous development of immune function differently among species remains unstudied. In this study, we examined the ontogeny of constitutive immunity in relation to developmental stage in a group of 22 Passerine bird species. Our results show that inter-specific variation in immune activity at hatching was mainly explained by extrinsic factors mediated by the mother, suggesting an important role of maternal effects on offspring immunity at hatching. Activity of constitutive components of the immune defense was detected as early as 1-3 days post-hatching, and increasing with age, indicating that immune function in older nestlings reflects intrinsic development. Our results highlight both endogenous immune activity of altricial nestlings at an early developmental stage, and maternal effects on the ontogeny of immune function of young birds.
Department of Ecology and Evolutionary Biology
The temporal dynamics of immune gene expression and pathogen load reveal resistance and tolerance of bacteria infection by trans-generationally primed flour beetles
Author(s): Tate, AT, Andolfatto, P, Graham, AL
Immune priming allows individuals previously exposed to a pathogen to enjoy reduced susceptibility and higher survival probability upon re-exposure, compared to naïve cohorts. The protection can even be transferred across generations, but currently very little is known about the mechanisms that confer a primed immune response in invertebrates. Furthermore, whether trans-generational immune priming increases resistance (ability to kill pathogens), tolerance (ability to minimize or repair damage), or both is unknown. In trans-generational priming experiments reported here, we infected the larval offspring of naïve, sterilely wounded, or bacteria-challenged (primed) adult female beetles (Tribolium castaneum) with the bacterial entomopathogen Bacillus thuringiensis (Bt) and used DNA microarrays and qPCR to investigate the influence of maternal treatment on the temporal dynamics of bacterial load and immune gene expression. Meanwhile, we monitored the survival and development of infected and uninfected larvae from these treatments to quantify the functional outcomes of priming in this system. Initially, primed larvae were better able to curb bacterial proliferation and they subsequently exhibited increased tolerance for high bacterial loads. Moreover, primed larvae had better survival odds and buffered developmental costs of infection. Taken together, these results suggest that invertebrate immune priming is not just an outcome of more efficient microbe killing, as previously supposed, but rather a two-pronged reduction in the overall negative consequences of infection for the host, with broad implications for the evolution of immune priming and pathogen virulence strategies.
Institute of Biology
Transcriptome analysis of immune priming in the bumblebee (Bombus terrestris)
Author(s): Lattorff, M, Flemming, T
The innate immune system of invertebrates has been claimed to be unspecifically acting against saprophytes based on the observation, that the genes contributing to innate immunity are well conserved across species. However, in recent years specificity and a form of memory in invertebrate immunity (immune priming) have been shown to occur in a number of species. Homologous infections led to higher survival than heterologous infections. Especially long lived species that might be at risk of subsequent infections might have a selective advantage when developing a potentially costly immune response that shows specificity and longevity. As the underlying mechanisms of immune priming are not properly examined and understood we used a transcriptome analysis of heterologous and homologous infections using gram-positive and -negative bacteria in the bumblebee, Bombus terrestris. The results indicate that the gene expression pattern are determined by initial infections rather than by secondary pathogen exposure. Thus, the immune system is primed by the first pathogen to be encountered and shows a long-lasting response at the level of gene expression. Effector genes of the innate immune system pathways (e.g. antimicrobial peptides), which are differentially activated by gram-positive and -negative bacteria, do show a specific, long-lasting response initiated by the initial infections. Using a transcriptomic approach we are able to unravel the mechanism of immune priming in insects. Initial infections are indeed priming the immune response so that a secondary homologous infection might be better counteracted due to specifically expressed genes of the immune system than a heterologous infection.