scholarly journals Different effects of paternal trans-generational immune priming on survival and immunity in step and genetic offspring

2014 ◽  
Vol 281 (1797) ◽  
pp. 20142089 ◽  
Author(s):  
Hendrik Eggert ◽  
Joachim Kurtz ◽  
Maike F. Diddens-de Buhr

Paternal trans-generational immune priming, whereby fathers provide immune protection to offspring, has been demonstrated in the red flour beetle Tribolium castaneum exposed to the insect pathogen Bacillus thuringiensis . It is currently unclear how such protection is transferred, as in contrast to mothers, fathers do not directly provide offspring with a large amount of substances. In addition to sperm, male flour beetles transfer seminal fluids in a spermatophore to females during copulation. Depending on whether paternal trans-generational immune priming is mediated by sperm or seminal fluids, it is expected to either affect only the genetic offspring of a male, or also their step offspring that are sired by another male. We therefore conducted a double-mating experiment and found that only the genetic offspring of an immune primed male show enhanced survival upon bacterial challenge, while phenoloxidase activity, an important insect immune trait, and the expression of the immune receptor PGRP were increased in all offspring. This indicates that information leading to enhanced survival upon pathogen exposure is transferred via sperm, and thus potentially constitutes an epigenetic effect, whereas substances transferred with the seminal fluid could have an additional influence on offspring immune traits and immunological alertness.

2017 ◽  
Vol 29 (7) ◽  
pp. 1401 ◽  
Author(s):  
A. M. Edwards ◽  
E. Z. Cameron

The differential allocation hypothesis suggests that a mother should adjust the sex of offspring in relation to her mate’s attractiveness, thereby increasing future reproductive fitness when her sons inherit the attractive traits. More attractive males have been shown to sire more sons, but it is possible that the sex ratio skew could be a result of paternal rather than maternal manipulation, which would be a more parsimonious explanation. We manipulated coital rate (an indicator of attractiveness) in laboratory mice and showed that males that mate more often have higher levels of glucose in their semen despite lower blood glucose levels. Since peri-conceptual glucose levels in utero increase male conceptus survival, this could result in male-biased sex ratios. The males that mated most also had more remaining X-chromosome-bearing-spermatozoa, suggesting depletion of Y-chromosome-bearing-spermatozoa during mating. We hypothesise that males may alter both seminal fluids and X : Y ratios in an ejaculate to influence subsequent sex ratios. Our results further support a paternal role in sex allocation.


2018 ◽  
Author(s):  
Imroze Khan ◽  
Arun Prakash ◽  
Deepa Agashe

AbstractIn many insects, individuals primed with low doses of pathogens live longer after being exposed to the same pathogen later in life. Yet, our understanding of the evolutionary and ecological history of priming of immune response in natural insect populations is limited. Previous work demonstrated population-, sex- and- stage specific variation in the survival benefit of priming response in flour beetles (Tribolium castaneum) infected with their natural pathogenBacillus thuringiensis. However, the evolutionary forces responsible for this natural variation remained unclear. Here, we tested whether the strength of the priming response (measured as the survival benefit after priming and subsequent infection relative to unprimed controls) was associated with multiple fitness parameters across 10 flour beetle populations. Our results suggest two major selective pressures that may explain the observed inter-population variation in priming: (A) Basal pathogen susceptibility – populations that were more susceptible to infection produced a stronger priming response, and (B) Reproductive success – populations where primed females produced more offspring had lower survival benefit, suggesting a trade-off between priming response and reproduction. Our work is the first empirical demonstration of multiple selective pressures that may govern the adaptive evolution of immune priming in the wild. We hope that this motivates further experiments to establish the role of pathogen-imposed selection and fitness costs in the evolution of priming in natural insect populations.


2019 ◽  
Author(s):  
Arun Prakash ◽  
Deepa Agashe ◽  
Imroze Khan

ABSTRACTInsects exhibit various forms of immune responses, including basal resistance to pathogens and a form of immune memory (“priming”) that can act within or across generations. The evolutionary drivers of such diverse immune functions remain poorly understood. Previously, we found that in the beetle Tribolium castaneum, both resistance and priming evolved as mutually exclusive strategies against the pathogen Bacillus thuringiensis. However, since evolved resistance improved survival far more than priming, the evolution of priming in some populations was puzzling. Was resistance more costly in these populations, or did priming provide added benefits? To test this, we revisited our evolved beetles and analyzed the costs and benefits of evolved priming vs. resistance. Surprisingly, resistant beetles increased reproduction after infection, with no measurable costs. In contrast, mounting a priming response reduced offspring early survival, development rate and reproduction. Even added trans-generational survival benefits of evolved priming could not tilt the balance in favor of priming. Hence, resistance is consistently more beneficial than priming; and the evolution and persistence of costly priming rather than resistance remains a mystery. Nevertheless, our work provides the first detailed comparison of the complex fitness consequences of distinct insect immune strategies, opening new questions about their evolutionary dynamics.


2020 ◽  
Author(s):  
Somadina I Okwelogu ◽  
Joseph I Ikechebelu ◽  
Nneka R Agbakoba ◽  
Kingsley C Anukam

AbstractBacterial infections are usually suspected in infertile couples seeking IVF with no clear understanding of the microbial compositions present in the seminal fluids and vaginal swabs of the patients. We used next-generation sequencing technology to correlate microbiota compositions with IVF clinical outcomes. Thirty-six couples were recruited to provide seminal fluids and vaginal swabs. Seminal fluid microbiota compositions had lower bacterial concentrations compared with the vagina, but species diversity was significantly higher in seminal fluid samples. Azoospermic subjects had more relative abundance of Mycoplasma and Ureaplasma. In Normospermic semen Lactobacillus (43.86%) was the most abundant, followed by Gardnerella (25.45%), while the corresponding vaginal samples, Lactobacillus (61.74%) was the most abundant, followed by Prevotella (6.07%), and Gardnerella (5.86%). Semen samples with positive IVF were significantly colonized by Lactobacillus jensenii (P=0.002), Faecalibacterium (P=0.042) and significantly less colonized by Proteobacteria, Prevotella, Bacteroides and lower Firmicutes/Bacteroidetes ratio compared with semen samples with negative IVF. Vaginal samples with positive IVF clinical outcome were significantly colonized by Lactobacillus gasseri, less colonized by Bacteroides, and Lactobacillus iners. This study has opened a window of possibility for Lactobacillus replenishments in men and women prior to IVF treatment.


2021 ◽  
Author(s):  
Lai Ka Lo ◽  
Reshma R ◽  
Lisa-Johanna Tewes ◽  
Barbara Milutinović ◽  
Caroline Müller ◽  
...  

Rapid recognition of disease cues is essential for preventing pathogenic infections and for disease management in group-living animals. Healthy individuals across taxa can detect illness in other conspecifics and adjust their responses to limit further infections of themselves and the group. However, little is known about potential changes in chemical phenotypes due to disease, which may mediate these responses. We here asked whether individual immune experience resulting from wounding or the injection of heat-killed bacteria of Bacillus thuringiensis (i.e., immune priming) leads to changes in the chemical profiles of adult red flour beetles (Tribolium castaneum). This group-living insect species is a well-studied example for both immune priming as a form of innate immune memory and niche construction via 'external immunity', i.e., the secretion of quinone-containing antimicrobials into the flour. Upon interaction with wounded conspecifics, naive beetles were previously found to not only up-regulate immunity, but moreover reduce gene expression of the evolutionary capacitor HSP90, an effect that has the potential to enhance adaptability. We here used gas chromatography-flame-ionisation detection (GC-FID) to study the composition of stink gland secretions and cuticular hydrocarbons (CHCs) of immune-primed and wounded beetles compared to controls. The overall profiles as well as target compounds of the stink gland secretions showed transient, slight changes after these treatments, particularly in wounded females. Priming and wounding led to pronounced changes in CHC profiles with increases in the proportion of methyl-branched alkanes. Furthermore, we found sex-specific differences, that were particularly pronounced in the CHCs, although the changes due to immune stimulation were overall similar in both sexes. We suggest that CHCs are potential candidates for the transfer of information related to individual immunological experience into the group.


2017 ◽  
Author(s):  
Imroze Khan ◽  
Arun Prakash ◽  
Deepa Agashe

ABSTRACTUnder strong pathogen pressure, insects often evolve resistance to infection. Many insects are also protected via immune memory (‘immune priming’), whereby sub-lethal exposure to a pathogen enhances survival after secondary infection. To understand the evolution and consequences of these immune responses, we imposed strong pathogen selection on flour beetles (Tribolium castaneum), infecting them with Bacillus thuringiensis (Bt) for 11 generations. Populations injected first with heat-killed and then live Bt each generation evolved high basal resistance against multiple Bt strains. In contrast, all populations injected only with a high dose of live Bt evolved less effective but strain-specific priming response. Control populations injected with heat-killed Bt did not evolve priming; and in the ancestor, priming was effective only against a low Bt dose. Thus, pathogens can select for rapid modulation of insect priming ability, leading to divergent immune strategies (generalized resistance vs. specific immune priming) with distinct mechanisms and adaptive benefits.


Author(s):  
Somadina I. Okwelogu ◽  
Joseph I. Ikechebelu ◽  
Nneka R. Agbakoba ◽  
Kingsley C. Anukam

BackgroundBacterial infections are usually suspected in infertile couples seeking IVF with no clear understanding of the microbial compositions present in the seminal fluids and vaginal niche of the patients. We used next-generation sequencing technology to correlate microbiota compositions with IVF clinical outcomes.MethodsThirty-six couples were recruited to provide seminal fluids and vaginal swabs. Bacterial DNA was extracted, and V4 region of the 16S rRNA was amplified and sequenced in a pair-end configuration on the Illumina MiSeq platform rendering 2 × 150 bp sequences. Microbial taxonomy to species level was generated using the Greengenes database. Linear discriminant analysis (LDA) effect size (LEfSe) was used to identify biologically and statistically significant differences in relative abundance.ResultsSeminal fluid microbiota compositions had lower bacterial concentrations compared with the vagina, but species diversity was significantly higher in seminal fluid samples. Azoospermic subjects had more relative abundance of Mycoplasma and Ureaplasma. In Normospermic semen, Lactobacillus (43.86%) was the most abundant, followed by Gardnerella (25.45%), while the corresponding vaginal samples, Lactobacillus (61.74%) was the most abundant, followed by Prevotella (6.07%) and Gardnerella (5.86%).ConclusionsSemen samples with positive IVF were significantly colonized by Lactobacillus jensenii (P=0.002), Faecalibacterium (P=0.042) and significantly less colonized by Proteobacteria, Prevotella, Bacteroides, and lower Firmicutes/Bacteroidetes ratio compared with semen samples with negative IVF. Vaginal samples with positive IVF clinical outcome were significantly colonized by Lactobacillus gasseri, less colonized by Bacteroides and Lactobacillus iners. This study has opened a window of possibility for Lactobacillus replenishments in men and women before IVF treatment.


2014 ◽  
Vol 281 (1785) ◽  
pp. 20140454 ◽  
Author(s):  
Javier Hernández López ◽  
Wolfgang Schuehly ◽  
Karl Crailsheim ◽  
Ulrike Riessberger-Gallé

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.


2019 ◽  
Vol 4 (1) ◽  
pp. 59-76 ◽  
Author(s):  
Alison E. Fowler ◽  
Rebecca E. Irwin ◽  
Lynn S. Adler

Parasites are linked to the decline of some bee populations; thus, understanding defense mechanisms has important implications for bee health. Recent advances have improved our understanding of factors mediating bee health ranging from molecular to landscape scales, but often as disparate literatures. Here, we bring together these fields and summarize our current understanding of bee defense mechanisms including immunity, immunization, and transgenerational immune priming in social and solitary species. Additionally, the characterization of microbial diversity and function in some bee taxa has shed light on the importance of microbes for bee health, but we lack information that links microbial communities to parasite infection in most bee species. Studies are beginning to identify how bee defense mechanisms are affected by stressors such as poor-quality diets and pesticides, but further research on this topic is needed. We discuss how integrating research on host traits, microbial partners, and nutrition, as well as improving our knowledge base on wild and semi-social bees, will help inform future research, conservation efforts, and management.


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