Within and transgenerational immune priming in an insect to a DNA virus

Tidbury, Hannah J.; Pedersen, Amy B.; Boots, Mike

doi:10.1098/rspb.2010.1517

Cited by 139 publications

(152 citation statements)

References 41 publications

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“…We also found that a protective effect of prior treatment with a small dose of the pathogen ('priming') extends for 7 days [previous experiments in this system had only looked for immediate effects and those 2 days following priming exposure (McTaggart et al, 2012)]. This is comparable with the observations of priming after 8 days in beetles (Roth et al, 2009) and 6 days in moths (Tidbury et al, 2011) and shows that priming of the innate system is relatively persistent. This persistent priming also has broad implications for understanding the epidemiological consequences of priming.…”

Section: Research Articlesupporting

confidence: 84%

The development of pathogen resistance in Daphnia magna: implications for disease spread in age-structured populations

Garbutt

O'Donoghue

McTaggart

et al. 2014

Journal of Experimental Biology

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Immunity in vertebrates is well established to develop with time, but the ontogeny of defence in invertebrates is markedly less studied. Yet, age-specific capacity for defence against pathogens, coupled with age structure in populations, has widespread implications for disease spread. Thus, we sought to determine the susceptibility of hosts of different ages in an experimental invertebrate host-pathogen system. In a series of experiments, we show that the ability of Daphnia magna to resist its natural bacterial pathogen Pasteuria ramosa changes with host age. Clonal differences make it difficult to draw general conclusions, but the majority of observations indicate that resistance increases early in the life of D. magna, consistent with the idea that the defence system develops with time. Immediately following this, at about the time when a daphnid would be most heavily investing in reproduction, resistance tends to decline. Because many ecological factors influence the age structure of Daphnia populations, our results highlight a broad mechanism by which ecological context can affect disease epidemiology. We also show that a previously observed protective effect of restricted maternal food persists throughout the entire juvenile period, and that the protective effect of prior treatment with a small dose of the pathogen ('priming') persists for 7 days, observations that reinforce the idea that immunity in D. magna can change over time. Together, our experiments lead us to conclude that invertebrate defence capabilities have an ontogeny that merits consideration with respect to both their immune systems and the epidemic spread of infection.

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Section: Research Articlesupporting

confidence: 84%

The development of pathogen resistance in Daphnia magna: implications for disease spread in age-structured populations

Garbutt

O'Donoghue

McTaggart

et al. 2014

Journal of Experimental Biology

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“…Because of the trade-off between current egg production and egg protection, TGIP might be expected in iteroparous species rather than in semelparous ones. In line with this, TGIP has been evidenced in iteroparous arthropods [3,4,[9][10][11][12][13][14]35] and not in semelparous ones [36,37]. Iteroparity could allow females to adjust their relative investment into egg protection compared with egg production in accordance to the risk of infection of the progeny and their own risk of dying from the infection.…”

Section: Discussionmentioning

confidence: 81%

Relationship between maternal transfer of immunity and mother fecundity in an insect

et al. 2012

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Trans-generational immune priming (TGIP) corresponds to the plastic adjustment of offspring immunity as a result of maternal immune experience. TGIP is expected to improve mother's fitness by improving offspring individual performance in an environment where parasitism becomes more prevalent. However, it was recently demonstrated that maternal transfer of immunity to the offspring is costly for immunechallenged female insects. Thus, these females might not provide immune protection to all their offspring because of the inherent cost of other fitness-related traits. Females are therefore expected to adjust their investment to individual offspring immune protection in ways that maximize their fitness. In this study, we investigated how bacterially immune-challenged females of the mealworm beetle, Tenebrio molitor, provision their eggs with immune protection according to egg production. We found that immunechallenged females provide a variable number of their eggs with internal antibacterial activity along egg-laying bouts. Furthermore, within the first immune-protected egg-laying bout (2 -4 days after the maternal immune challenge), the number of eggs protected was strongly dependent on the number of eggs produced. Immune-challenged females might therefore adjust their investment into TGIP and fecundity according of their individual perception of the risk of dying from the infection and the expected parasitic conditions for the offspring.

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“…Similar long-term beneficial effects have also been described for maternal antibodies, which induce T-celldependent idiotypic responses during the neonatal period (3). In addition, transgenerational immune priming has been demonstrated in insects challenged with bacteria or viruses (37,38). Maternally transmitted susceptibility for trypanosome infections has also been described in tsetse (39)(40)(41).…”

Section: Discussionmentioning

confidence: 99%

PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse’s offspring

Wang

Aksoy

2012

Proc. Natl. Acad. Sci. U.S.A.

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Beneficial microbe functions range from host dietary supplementation to development and maintenance of host immune system. In mammals, newborn progeny are quickly colonized with a symbiotic fauna that is provisioned in mother's milk and that closely resembles that of the parent. Tsetse fly (Diptera: Glossinidae) also depends on the obligate symbiont Wigglesworthia for nutritional supplementation, optimal fecundity, and immune system development. Tsetse progeny develop one at a time in an intrauterine environment and receive nourishment and symbionts in mother's milk. We show that the host Peptidoglycan Recognition Protein (PGRP-LB) is expressed only in adults and is a major component of the milk that nourishes the developing progeny. The amidase activity associated with PGRP-LB may scavenge the symbiotic peptidoglycan and prevent the induction of tsetse's Immune Deficiency pathway that otherwise can damage the symbionts. Reduction of PGRP-LB experimentally diminishes female fecundity and damages Wigglesworthia in the milk through induction of antimicrobial peptides, including Attacin. Larvae that receive less maternal PGRP-LB give rise to adults with fewer Wigglesworthia and hyperimmune responses. Such adults also suffer dysregulated immunity, as indicated by the presence of higher trypanosome densities in parasitized adults. We show that recPGRP-LB has antimicrobial and antitrypanosomal activities that may regulate symbiosis and impact immunity. Thus, PGRP-LB plays a pivotal role in tsetse's fitness by protecting symbiosis against host-inflicted damage during development and by controlling parasite infections in adults that can otherwise reduce host fecundity. maternal transfer | transgenerational immune effects | antimicrobial activity | antitrypanosomal activity

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Within and transgenerational immune priming in an insect to a DNA virus

Cited by 139 publications

References 41 publications

The development of pathogen resistance in Daphnia magna: implications for disease spread in age-structured populations

The development of pathogen resistance in Daphnia magna: implications for disease spread in age-structured populations

Relationship between maternal transfer of immunity and mother fecundity in an insect

PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse’s offspring

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