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.
Bi-parental immune priming in the sex-role reversed pipefish Syngnathus typhle
Author(s): Beemelmanns, A, Roth, O
The transfer of immunity from mothers to offspring (trans-generational immune priming) yields in an improved offspring immunity and an induced parasite resistance. In teleost this occurs via maternal deposition of antibodies into the egg yolk. As yet, the paternal contribution to offspring immunity was suggested to be negligible because sperm are too small for a transfer over the scope of the DNA.
Syngnathids like the sex-role reversed pipefish Syngnathus typhle have evolved a paternal placenta-like structure, in which embryos are nursed. This gives a mechanistic opportunity for paternal transfer of immunity but also implies that offspring are born in the paternal environment and thus share a similar parasite pressure. Hence, strong selection for the evolution of paternal immune priming can be expected.
We experimentally investigated the potential of maternal, paternal and bi-parental immune priming on offspring cell activity and gene expression patterns. We found that offspring’s immune defence was enhanced upon parental bacteria exposure, independent of whether mother, father or both were challenged. This suggests that male pregnancy let to the evolution of bi-parental immune priming. Classically, maternal immune priming is considered to be of higher importance due to the fact that mothers invest more resources in production and care of offspring. However, since in sex-role reversal males do not only have an intense paternal investment but also realize evolutionary maternal traits like a more efficient immune response, selection pressures for paternal immune priming should be stronger. As immune priming is expected to be energetically costly for both parents and offspring, life history parameters provide clarification about incorporated costs and benefits. Further, future data will give insights in the mechanistic basis of bi-parental immune priming and assess what role antibodies, innate immunity and epigenetics play.
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 Evolutionary Ecology
Context-dependent paternal effects of infection on offspring survival and condition
Author(s): Kaufmann, JP, Lenz, TL, Milinski, M, Eizaguirre, C
Besides traditional genetic inheritance, the phenotype of an individual can be influenced by its parents’ phenotypes and environment. Whether those environmentally-induced parental effects are adaptive though remains elusive. To address this question, we focused on paternal effects of exposure to a nematode parasite in the three-spined stickleback. We experimentally investigated how parasite infection affects adult stickleback males and their offspring’s early life history traits and parasite resistance. By means of in vitro fertilization, we produced over 50 maternal half-sibships sired by pairs of infected and uninfected brothers. We first present evidence for sperm deficiency in infected fathers compared to uninfected fathers (reduced velocity and fertilizing ability). We then show that although offspring of infected fathers suffered from low hatching success and survival rates, when exposed to the same parasite, they achieved higher body condition than their counterparts from uninfected fathers. These results highlight that the adaptive potential for paternal effects is only expressed in the presence of the paternal environmental stressor. We thus discuss the likelihood and potential consequences of sperm-mediated transgenerational effects under stable or predictable environments.
Epidemiological and evolutionary implications of immune priming
Author(s): Boots, M
The body of empirical evidence for immune priming in invertebrates is growing. To highlight this, here, I will give an example of within and transgenerational priming in an insect to challenge by a natural DNA virus. Given this widespread phenomena and the fact that priming, defined here as immunity following challenge to a pathogen, contrasts epidemiologically with acquired immunity which occurs after recovery from an infectious state, it is important to model the implications of priming. Defined in this way priming can also be a characteristic of vertebrate immunity. Here I will describe the epidemiological and evolutionary characteristics of a SPI (susceptible:primed:infectious) model as distinct from the SIR (susceptible:infected:recovered/removed) model of acquired immunity. The models highlight the potential importance of priming to the epidemiology and evolution of host parasite interactions.
CEFE-CNRS UMR 5175
Evolution of a transgenerational response to parasites, the maternal transfer of antibodies: theory, experiments and comparative approaches
Author(s): Boulinier, T, Garnier, R, Ramos, R, Gandon, S
Among the many responses that hosts show against parasites, the transgenerational transfer of immunity is now receiving increased attention due to its broad potential evolutionary, epidemiological and ecological implications. In vertebrates, the maternal transfer of antibodies is a transgenerational response to parasites for which there is a relatively strong mechanistic and biomedical understanding of the processes involved. Recent theoretical work and experiments we conducted to address evolutionary predictions are nevertheless shedding new light on both the proximate and ultimate processes involved. We notably found that the temporal persistence of maternal antibodies in young birds after hatching can be much longer than previously thought, and that this persistence is predictably linked to the life history of the considered species. Because of the mechanistic link between antibody persistence in adults and young, this has implication for the evolution of acquired immunity. We also showed that offspring can receive maternal antibodies via allosuckling in social mammals. Such results have wide implications, from comparative immunology and the evolution of social behaviours, to the use of vaccines as management tools in eco-epidemiology. They also call for further work at the interface between mechanistic and evolutionary approaches.
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.
Ecology & Evolutionary Biology
Immune-based maternal effects in response to experimental manipulation of bacterial load in tree swallow nests
Author(s): Forsman, AM
Birds encounter a variety of bacteria in their environment on a daily basis. The vast majority of these organisms likely exert minimal direct effects on avian fitness, while others may exert negative pathogenic effects or conversely, positive probiotic effects. Regardless of pathogenicity, the antigenic properties of many bacteria likely contribute to variation in immune status among individual birds at any given time. Some of this variation may in turn be inherited from mother to offspring through the deposition of protective immune compounds into eggs. Neonates may be especially sensitive to environmental bacteria during the first weeks of life, before the immune system is fully developed and the gut microbiota established. And thus, variation in female exposure to bacteria prior to egg-laying may result in indirect fitness consequences through maternal effects on early offspring immune phenotype. In this study, I manipulated bacterial load in tree swallow nests during nest-building and egg-laying to explore bacterial effects on female investment in egg defenses and on offspring growth and immune status. Contrary to my predictions, eggs collected from nestboxes with added bacteria contained lower concentrations and total amounts of yolk antibodies than eggs from control nests. These patterns, observed for total yolk antibodies, were also reflected in nestling plasma samples. Nestlings whose mothers were exposed to increased bacterial load also exhibited lower bactericidal capacity than control nestlings at six days post-hatch, but not at twelve days post-hatch. No differences in nestling size, growth, or PHA responsiveness were observed among treatment groups.
Department of Zoology
Maternal immune challenges exert both enhancing and suppressive effects on offspring immune responses
Author(s): Grindstaff, JL, Merrill, L
Maternal antibodies can both enhance and suppress offspring humoral immune responses. However, these enhancing and suppressive effects have typically been documented in separate studies conducted with different species and different antigens over variable time periods. Thus the conditions that induce a priming effect of maternal immune challenge versus a suppressive effect have been unclear. In this study, we exposed female zebra finches (Taeniopygia guttata) and their offspring to one of two antigens (keyhole limpet hemocyanin (KLH) or lipopolysaccharide (LPS)) or a control treatment and quantified maternal antibody transmission and endogenous offspring antibody production. Antigen-specific maternal antibodies reached their lowest levels between days 17 and 28 post-hatch and total antibody concentrations peaked at day 17 post-hatch. We found that both maternal KLH and maternal LPS exposure stimulated the production of antigen-specific antibodies in non-challenged offspring after the catabolism of maternal antibodies. This suggests a stimulatory effect of maternal immune challenge on offspring humoral immunity. However, offspring of both KLH and LPS challenged mothers exhibited weaker antigen-specific secondary immune responses when mothers and offspring were challenged with the same antigen. Maternal immune challenge did not impact the ability of young to respond to the other antigen. This supports a specific, suppressive effect of maternal immune challenge on offspring antibody production. Thus, maternal antibodies can have an instructive role, potentially acting as internal antigens, and stimulate offspring antigen-specific antibody production in response to two distinct antigens. However, when the early antigenic environment of offspring is similar to the maternal antigenic environment, maternal antibodies may suppress the endogenous antibody responses of young.
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