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1.
It is widely acknowledged that a mother, and the maternal environment, can have a profound effect on the phenotype of her offspring. For example, immunocompetent vertebrate mothers can pass on immune factors to their otherwise immune na?ve offspring. Recently, it has also been demonstrated in invertebrates that maternal contact with pathogens and immune elicitors can have a positive impact on offspring resistance and immune system components. Here, using a cross-fostering design, we show that trans-generational immune priming in a social insect, similar to birds, takes place through factors in the eggs, with effects persisting into adult worker offspring. Additionally, eggs from immune-challenged mothers are imbued with increased internal antibacterial activity when they are laid.  相似文献   

2.
Parasites impose different selection regimes on their hosts, which respond by increasing their resistance and/or tolerance. Parental challenge with parasites can enhance the immune response of their offspring, a phenomenon documented in invertebrates and termed transgenerational immune priming. We exposed two parental generations of the model organism Daphnia magna to the horizontally transmitted parasitic yeast Metschnikowia bicuspidata and recorded resistance- and tolerance-related traits in the offspring generation. We hypothesized that parentally primed offspring will increase either their resistance or their tolerance to the parasite. Our susceptibility assays revealed no impact of parental exposure on offspring resistance. Nonetheless, different fitness-related traits, which are indicative of tolerance, were altered. Specifically, maternal priming increased offspring production and decreased survival. Grandmaternal priming positively affected age at first reproduction and negatively affected brood size at first reproduction. Interestingly, both maternal and grandmaternal priming significantly reduced within-host–parasite proliferation. Nevertheless, Daphnia primed for two consecutive generations had no competitive advantage in comparison to unprimed ones, implying additive maternal and grandmaternal effects. Our findings do not support evidence of transgenerational immune priming from bacterial infections in the same host species, thus, emphasizing that transgenerational immune responses may not be consistent even within the same host species.  相似文献   

3.
Natural selection should favour parents that are able to adjust their offspring's life-history strategy and resource allocation in response to changing environmental and social conditions. Pathogens impose particularly strong and variable selective pressure on host life histories, and parental genes will benefit if offspring are appropriately primed to meet the immunological challenges ahead. Here, we investigated transgenerational immune priming by examining reproductive resource allocation by female mice in response to direct infection with Babesia microti prior to pregnancy. Female mice previously infected with B. microti gained more weight over pregnancy, and spent more time nursing their offspring. These offspring generated an accelerated response to B. microti as adults, clearing the infection sooner and losing less weight as a result of infection. They also showed an altered hormonal response to novel social environments, decreasing instead of increasing testosterone production upon social housing. These results suggest that a dominance-resistance trade-off can be mediated by cues from the previous generation. We suggest that strategic maternal investment in response to an infection leads to increased disease resistance in the following generation. Offspring from previously infected mothers downregulate investment in acquisition of social dominance, which in natural systems would reduce access to mating opportunities. In doing so, however, they avoid the reduced disease resistance associated with increased testosterone and dominance. The benefits of accelerated clearance of infection and reduced weight loss during infection may outweigh costs associated with reduced social dominance in an environment where the risk of disease is high.  相似文献   

4.
Maternal effects can be adaptive and because of their intrinsic time delays may have important effects on population dynamics. In vertebrates, and increasingly invertebrates, it is well established that offspring defence is in part determined by maternal parasite exposure. It has also been suggested that there may be indirect maternal effects on immunity mediated by other components of the maternal environment, including density and resource availability. Here, we examine the effect maternal resource availability has on the immunity of offspring in an insect-virus system. We use five different maternal resource levels and examine immunity in the offspring both directly, by challenge with a virus, and by measuring a major component of the immune system, across three offspring environments. Both the direct infection assay and the measure of immunocompetence show clearly that offspring from mothers in poor environments are more resistant to parasites. This may result from life-history optimization of mothers in poor environments, or because the poor environment acts as a cue for higher disease risk in the next generation. This emphasizes the importance of maternal effects on disease resistance, mediated through indirect environmental factors that will have important implications to both the ecological and evolutionary dynamics of host-parasite interactions.  相似文献   

5.
Transgenerational effects of infection have a huge potential to influence the prevalence and intensity of infections in vectors and, by extension, disease epidemiology. These transgenerational effects may increase the fitness of offspring through the transfer of protective immune factors. Alternatively, however, infected mothers may transfer the costs of infection to their offspring. Although transgenerational immune protection has been described in a dozen invertebrate species, we still lack a complete picture of the incidence and importance of transgenerational effects of infection in most invertebrate groups. The existence of transgenerational infection effects in mosquito vectors is of particular interest because of their potential for influencing parasite prevalence and intensity and, by extension, disease transmission. Here we present what we believe to be the first study on transgenerational infection effects in a mosquito vector infected with malaria parasites. The aim of this experiment was to quantify both the benefits and the costs of having an infected mother. We find no evidence of transgenerational protection in response to a Plasmodium infection. Having an infected mother does, however, entail considerable fecundity costs for the offspring: fecundity loss is three times higher in infected offspring issued from infected mothers than in infected offspring issued from uninfected mothers. We discuss the implications of our results and we call for more studies looking at transgenerational effects of infection in disease vectors.  相似文献   

6.
Little is known about the maternal transfer of antibodies in natural host-parasite systems despite its possible evolutionary and ecological implications. In domestic animals, the maternal transfer of antibodies can enhance offspring survival via a temporary protection against parasites, but it can also interfere with the juvenile immune response to antigens. We tested the functional role of maternal antibodies in a natural population of a long-lived colonial seabird, the kittiwake (Rissa tridactyla), using a vaccine (Newcastle disease virus vaccine) to mimic parasite exposure combined with a cross-fostering design. We first investigated the role of prior maternal exposure on the interannual transmission of Ab to juveniles. We then tested the effect of these antibodies on the juvenile immune response to the same antigen. The results show that specific maternal antibodies were transferred to chicks 1 year after maternal exposure and that these antibodies were functional, i.e. they affected juvenile immunity. These results suggest that the role of maternal antibodies may depend on the timing and pattern of offspring exposure to parasites, along with the patterns of maternal exposure and the dynamics of her immune response. Overall, our approach underlines that although the transgenerational transfer of antibodies in natural populations is likely to have broad implications, the nature of these effects may vary dramatically among host-parasite systems, depending on the physiological mechanisms involved and the ecological context.  相似文献   

7.
Trans-generational immune priming in a social insect   总被引:3,自引:0,他引:3       下载免费PDF全文
Detecting functional homology between invertebrate and vertebrate immunity is of interest in terms of understanding the dynamics and evolution of immune systems. Trans-generational effects on immunity are well known from vertebrates, but their existence in invertebrates remains controversial. Earlier work on invertebrates has interpreted increased offspring resistance to pathogens as trans-generational immune priming. However, interpretation of these earlier studies involves some caveats and thus full evidence for a direct effect of maternal immune experience on offspring immunity is still lacking in invertebrates. Here we show that induced levels of antibacterial activity are higher in the worker offspring of the bumblebee, Bombus terrestris L. when their mother queen received a corresponding immune challenge prior to colony founding. This shows trans-generational immune priming in an insect, with ramifications for the evolution of sociality.  相似文献   

8.
Maternal effects by which females provide their offspring with non-genetic factors such as hormones, nutrients and antibodies can have an important impact on offspring fitness. In vertebrates, maternal antibodies (matAb) are transferred from the mother, via the placenta, egg yolk or milk during lactation to offspring until they are 2 weeks (birds), 4-10 weeks (rodents) and 9 months (humans) old, respectively. matAb transfer can have direct effects on offspring growth rate in birds and rodents, probably by passively protecting the newborn from common pathogens before their endogenous immune system has matured. Indirect long-term effects of matAb transfer on the offspring's own immunity can be synergistic, if matAb act as antigen templates of the accumulated immunological experience of the mother and educate the newborn's immune system. However, it may also be suppressive if matAb reduce antigen presentation to the newborn resulting in antigen-specific blocking of offspring endogenous immunity. Our aim is to review the mechanisms and direct effects of matAb transfer in vertebrates with an emphasis on birds, outline a framework for research on the long-term effects of matAb on the endogenous immune system of the mature offspring and encourage ecological and evolutionary studies of matAb transfer in non-domesticated animals.  相似文献   

9.
Trans‐generational immune priming is the transmission of enhanced immunity to offspring following a parental immune challenge. Although within‐generation increased investment into immunity demonstrates clear costs on reproductive investment in a number of taxa, the potential for immune priming to impact on offspring reproductive investment has not been thoroughly investigated. We explored the reproductive costs of immune priming in a field cricket, Teleogryllus oceanicus. To assess the relative importance of maternal and paternal immune status, mothers and fathers were immune‐challenged with live bacteria or a control solution and assigned to one of four treatments in which one parent, neither or both parents were immune‐challenged. Families of offspring were reared to adulthood under a food‐restricted diet, and approximately 10 offspring in each family were assayed for two measures of immunocompetence. We additionally quantified offspring reproductive investment using sperm viability for males and ovary mass for females. We demonstrate that parental immune challenge has significant consequences for the immunocompetence and, in turn, reproductive investment of their male offspring. A complex interaction between maternal and paternal immune status increased the antibacterial immune response of male offspring. This increased immune response was associated with a reduction in son's sperm viability, implicating a trans‐generational resource trade‐off between investment into immunocompetence and reproduction. Our data also show that these costs are sexually dimorphic, as daughters did not demonstrate a similar increase in immunity, despite showing a reduction in ovary mass.  相似文献   

10.
Transgenerational effects, whereby the environment experienced by a parent leads to an altered offspring phenotype, have now been described in a variety of taxa. In invertebrates, much of the research on these effects has concentrated on the role of parental exposure to pathogens or immune elicitors in determining offspring immune investment or disease resistance. To date, however, studies of transgenerational effects in invertebrates have generally been restricted to single infections or immune elicitors in ideal laboratory environments. Animals in field situations will commonly experience sub‐optimal environments and co‐infection by multiple species of parasites and pathogens, leading to increased relative costs of immune investment and changing fitness benefits from offspring responses to the parental environment. Here we investigate a more ecologically realistic scenario involving both multiple infections and resource limitation, using the Indian meal moth Plodia interpunctella as a model host, challenged with the entomopathogenic bacterium Bacillus thuringiensis and fungus Beauveria bassiana. Mothers were exposed to low doses of one or both pathogens, or a control. Offspring from each family were reared on either good‐ or poor‐quality food and then exposed to one or both pathogens. Maternal exposure to pathogens led to reduced pathogen resistance in offspring, depending on the combination of maternal and offspring pathogen‐specific infections and resource limitation in the offspring generation. Much research to date has focussed on trans‐generational immune priming, in which parental exposure to pathogens or immune elicitors leads to upregulated immune reactivity in their offspring. The lack of any such effects in our system suggests that the production of less resistant offspring following parental exposure to pathogens might be an important alternative, driven by costs of resistance rather than adaptive benefits.  相似文献   

11.
Effects of maternal environment on offspring performance have been documented frequently in herbivorous insects. Despite this, very few cases exist in which exposure of parent insects to a resource causes the phenotype of their offspring to be adjusted in a manner that is adaptive for that resource, a phenomenon called adaptive transgenerational phenotypic plasticity. I performed a two-generation reciprocal cross-transplant experiment in the field with the soft scale insect Saissetia coffeae (Hemiptera: Coccidae) on two disparate host plant species in order to separate genetic effects from possible transgenerational plasticity. Despite striking differences in quality between host species, maternal host had no effect on overall offspring performance, and I detected no "acclimatization" to the maternal host species. However, there was a significant negative association between maternal and offspring development times, with potentially adaptive implications. Furthermore, offspring of mothers reared in an environment where scale densities were higher and scales were more frequently killed by fungi were significantly less likely to suffer from fungal attack than were offspring of mothers reared in an environment where densities were low and fungal attack was rare. Although S. coffeae does not appear to alter offspring phenotype to increase offspring fitness on these two distinct plant species, it does appear that offspring phenotype may be responding to some subtler aspects of maternal environment. In particular, the possibility of induced transgenerational prophylaxis in S. coffeae deserves further investigation.  相似文献   

12.
1.?When parasitized, both vertebrates and invertebrates can enhance the immune defence of their offspring, although this transfer of immunity is achieved by different mechanisms. In some insects, immune-challenged males can also initiate trans-generational immune priming (TGIP), but its expressions appear qualitatively different from the one induced by females similarly challenged. 2.?The existence of male TGIP challenges the traditional view of the parental investment theory, which predicts that females should invest more into their progeny than males. However, sexual dimorphism in life-history strategies and the potential costs associated with TGIP may nevertheless lead to dissymmetric investment between males and females into the immune protection of the offspring. 3.?Using the yellow mealworm beetle, Tenebrio molitor, we show that after parental exposure to a bacterial-like infection, maternal and paternal TGIP are associated with the enhancement of different immune effectors and different fitness costs in the offspring. While all the offspring produced by challenged mothers had enhanced immune defence, only those from early reproductive episodes were immune primed by challenged fathers. 4.?Despite the fact that males and females may share a common interest in providing their offspring with an immune protection from the current pathogenic threat, they seem to have evolved different strategies concerning this investment.  相似文献   

13.
Parental investment theory postulates that adults can accurately perceive cues from their surroundings, anticipate the needs of future offspring based on those cues, and selectively allocate nongenetic resources to their progeny. Such context‐dependent parental contributions can result in phenotypically variable offspring. Consistent with these predictions, we show that bacterially exposed Manduca sexta mothers oviposited significantly more variable embryos (as measured by mass, volume, hatching time, and hatching success) relative to naïve and control mothers. By using an in vivo “clearance of infection” assay, we also show that challenged larvae born to heat‐killed‐ or live‐Serratia‐injected mothers, supported lower microbial loads and cleared the infection faster than progeny of control mothers. Our data support the notion that mothers can anticipate the future pathogenic risks and immunological needs of their unborn offspring, providing progeny with enhanced immune protection likely through transgenerational immune priming. Although the inclusion of live Serratia into oocytes does not appear to be the mechanism by which mothers confer protection to their young, other mechanisms, including epigenetic modifications in the progeny due to maternal pathogenic stress, may be at play. The adaptive nature of maternal effects in the face of pathogenic stress provides insights into parental investment, resource allocation, and life‐history theories and highlights the significant role that pathogen‐induced maternal effects play as generators and modulators of evolutionary change.  相似文献   

14.
15.
Eggs of vertebrates contain steroid hormones of maternal origin that may influence offspring performance. Recently, it has been shown that glucocorticoids, which are the main hormones mediating the stress response in vertebrates, are transmitted from the mother to the egg in birds. In addition, mothers with experimentally elevated corticosterone levels lay eggs with larger concentrations of the hormone, which produce slow growing offspring with high activity of the hypothalamo-adrenal axis under acute stress. However, the effects and function of transfer of maternal corticosterone to the eggs are largely unknown. In the present study, we injected corticosterone in freshly laid eggs of yellow-legged gulls (Larus michahellis), thus increasing the concentration of the hormone within its natural range of variation, and analyzed the effect of manipulation on behavioral, morphological, and immune traits of the offspring in the wild. Eggs injected with corticosterone had similar hatching success to controls, but hatched later. Mass loss during incubation was greater for corticosterone-treated eggs, except for the last laid ones. Corticosterone injection reduced rate and loudness of late embryonic vocalizations and the intensity of chick begging display. Tonic immobility response, reflecting innate fearfulness, was unaffected by hormone treatment. Elevated egg corticosterone concentrations depressed T-cell-mediated immunity but had no detectable effects on humoral immune response to a novel antigen, viability at day 10, or growth. Present results suggest that egg corticosterone can affect the behavior and immunity of offspring in birds and disclose a mechanism mediating early maternal effects whereby stress experienced by females may negatively translate to offspring phenotypic quality.  相似文献   

16.
The adaptive value of facultative maternal adjustment of offspring immunity, or trans-generational immune-priming, will depend on the ecological background. In particular, where there is a mismatch between the immune adjustment and offspring environment, the immunological link between mothers and offspring may be disadvantageous owing to the presence of associated costs. Costs to an individual of responding to an immune challenge are extensively documented. However, in addition to parents, the relevant costs for trans-generational immune-priming also pertain to offspring, but as yet it is unknown what costs offspring will bear. In bumble-bees, higher antibacterial activity has been shown as a trans-generational effect when mothers receive a bacterial-based immune challenge prior to colony founding. Here we show that while naive offspring from immune-challenged mothers do not show evidence for a direct energy-related survival cost, they do show increased susceptibility to a parasite distinctly unrelated to the maternal challenge. The presence of costs associated with trans-generational immune-priming will shape the evolution of this trait depending on the ecological setting.  相似文献   

17.
The transfer of acquired and specific immunity against previously encountered bacteria from mothers to offspring boosts the immune response of the next generation and supports the development of a successful pathogen defense. While most studies claim that the transfer of immunity is a maternal trait, in the sex‐role‐reversed pipefish Syngnathus typhle, fathers nurse the embryos over a placenta‐like structure, which opens the door for additional paternal immune priming. We examined the potential and persistence of bacteria‐type‐specific parental immune priming in the pipefish S. typhle over maturation time using a fully reciprocal design with two different bacteria species (Vibrio spp. and Tenacibaculum maritimum). Our results suggest that S. typhle is able to specifically prime the next generation against prevalent local bacteria and to a limited extent even also against newly introduced bacteria species. Long‐term protection was thereby maintained only against prevailing Vibrio bacteria. Maternal and paternal transgenerational immune priming can complement each other, as they affect different pathways of the offspring immune system and come with distinct degree of specificity. The differential regulation of DNA‐methylation genes upon parental bacteria exposure in premature pipefish offspring indicates that epigenetic regulation processes are involved in transferring immune‐related information across generations. The identified trade‐offs between immune priming and reproduction determine TGIP as a costly trait, which might constrain the evolution of long‐lasting TGIP, if parental and offspring generations do not share the same parasite assembly.  相似文献   

18.
Maternal antibodies (MatAb) are known to provide passive protection early in life for young vertebrates but their effects on the development of offspring immune response across generations are still unknown. Here, we investigated the effects of antigen exposure (keyhole limpet haemocyanin, KLH) experienced by urban pigeon (Columba livia) females on the amount of antigen-specific antibodies (Abs) transferred into the egg yolk of their daughters and on the humoural immune response towards this same antigen in their grandchildren. We found that chicks from KLH-injected maternal grandmothers had a higher humoural response than chicks from sham-injected grandmothers. However, we did not detect a significant effect of female KLH exposure on the ability of their daughters to transmit anti-KLH Abs into their eggs. These results suggest that antigen exposure at one generation may shape the immune profile of offspring over two next generations, although the underlying mechanisms remain to be investigated.  相似文献   

19.
Maternal effects, where the performance of offspring is determined by the condition of their mother, are widespread and may in some cases be adaptive. The crustacean Daphnia magna shows strong maternal effects: offspring size at birth and other proxies for fitness are altered when their mothers are older or when mothers have experienced dietary restriction. The mechanisms for this transgenerational transmission of maternal experience are unknown, but could include changes in epigenetic patterning. MicroRNAs (miRNAs) are regulators of gene expression that have been shown to play roles in intergenerational information transfer, and here, we test whether miRNAs are involved in D. magna maternal effects. We found that miRNAs were differentially expressed in mothers of different ages or nutritional state. We then examined miRNA expression in their eggs, their adult daughters and great granddaughters, which did not experience any treatments. The maternal (treatment) generation exhibited differential expression of miRNAs, as did their eggs, but this was reduced in adult daughters and lost by great granddaughters. Thus, miRNAs are a component of maternal provisioning, but do not appear to be the cause of transgenerational responses under these experimental conditions. MicroRNAs may act in tandem with egg provisioning (e.g., with carbohydrates or fats), and possibly other small RNAs or epigenetic modifications.  相似文献   

20.
Although evidence is accumulating that mothers can transfer antibodies to their offspring, little is known about the consequences of such a transfer to the offspring immune system. Because maternal antibodies are effective only during a short period of time after their transfer to offspring, one hypothesis is that maternal antibodies provides a transitory antigen-specific protection to offspring, thus lessening the need for offspring to mount their own humoral immune response towards these specific antigens. In birds, this scenario predicts that offspring immune response towards a specific antigen is inhibited to a larger extent in hatchlings than in older nestlings. We tested this hypothesis in tawny owls Strix aluco by cross-fostering clutches between nests and then challenging siblings with a vaccine either two times (at 4- and 11-d-old) or only one time at 11-d-old to compare the strength of the humoral response between nestlings born from mothers with naturally high and low levels of antibodies against this vaccine. Because maternal antibodies are expected to be effective only during a short period of time after hatching, we predict that maternal antibodies should inhibit the immune response of nestlings vaccinated from the fourth day after hatching more than in nestlings vaccinated only at a later age. As expected, the inhibitory effect of maternal antibodies was stronger in nestlings vaccinated soon after hatching than in siblings injected at a later age. Therefore, in wild avian populations pre-hatching maternal effects may confer offspring with a transitory immune protection in the first days following hatching.  相似文献   

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