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Parental legacy in insects: variation of transgenerational immune priming during offspring development.

ABSTRACT: In insects, a parental immune challenge can prepare and enhance offspring immune activity. Previous studies of such transgenerational immune priming (TGIP) mainly focused on a single offspring life stage. However, different developmental stages may be exposed to different risks and show different susceptibility to parental immune priming. Here we addressed the question (i) whether TGIP effects on the immunity of Manduca sexta offspring vary among the different developmental offspring stages. We differentiated between unchallenged and immunochallenged offspring; for the latter type of offspring, we further investigated (ii) whether TGIP has an impact on the time that enhanced immune levels persist after offspring immune challenge. Finally, we determined (iii) whether TGIP effects on offspring performance depend on the offspring stage. Our results show that TGIP effects on phenoloxidase (PO) activity, but not on antibacterial activity, vary among unchallenged offspring stages. In contrast, TGIP effects on PO and antibacterial activity did not vary among immunochallenged offspring stages. The persistence of enhanced immune levels in immunochallenged offspring was dependent on the parental immune state. Antibacterial (but not PO) activity in offspring of immunochallenged parents decreased over five days after pupal immune challenge, whereas no significant change over time was detectable in offspring of control parents. Finally, TGIP effects on the developmental time of unchallenged offspring varied among stages; young larvae of immunochallenged parents developed faster and gained more weight than larvae of control parents. However, offspring females of immunochallenged parents laid fewer eggs than females derived from control parents. These findings suggest that the benefits which the offspring gains from TGIP during juvenile development are paid by the adults with reduced reproductive power. Our study shows that TGIP effects vary among offspring stages and depend on the type of immunity (PO or antibacterial activity) as well as the time past offspring immune challenge.

SUBMITTER: Trauer U

PROVIDER: S-EPMC3658988 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:An insect's phenotype can be influenced by the experiences of the parental generation. However, the effects of the parental symbiotic microbiome and host plant use on the offspring are unclear. We addressed this gap of knowledge by studying Pieris brassicae, a multivoltine butterfly species feeding on different brassicaceous plants across generations. We investigated how disturbance of the parental bacterial community by antibiotic treatment affects F1 larval traits. We tested the effects depending on whether F1 larvae are feeding on the same plant species as their parents or on a different one. The parental treatment alone had no impact on the biomass of F1 larvae feeding on the parental plant species. However, the parental treatment had a detrimental effect on F1 larval biomass when F1 larvae had a different host plant than their parents. This effect was linked to higher larval prophenoloxidase activity and greater downregulation of the major allergen gene (MA), a glucosinolate detoxification gene of P. brassicae Bacterial abundance in untreated adult parents was high, while it was very low in F1 larvae from either parental type, and thus unlikely to directly influence larval traits. Our results suggest that transgenerational effects of the parental microbiome on the offspring's phenotype become evident when the offspring is exposed to a transgenerational host plant shift.IMPORTANCE Resident bacterial communities are almost absent in larvae of butterflies and thus are unlikely to affect their host. In contrast, adult butterflies contain conspicuous amounts of bacteria. While the host plant and immune state of adult parental butterflies are known to affect offspring traits, it has been unclear whether also the parental microbiome imposes direct effects on the offspring. Here, we show that disturbance of the bacterial community in parental butterflies by an antibiotic treatment has a detrimental effect on those offspring larvae feeding on a different host plant than their parents. Hence, the study indicates that disturbance of an insect's parental microbiome by an antibiotic treatment shapes how the offspring individuals can adjust themselves to a novel host plant.

Project description:Drought is the major abiotic stress that decreases plant water status, inhibits photosynthesis, induces oxidative stress, restricts growth and finally lead to the reduction of wheat yield. It has been proven that drought priming during vegetative growth stage could enhance tolerance to drought stress at grain filling in wheat. However, whether drought priming imposed at grain filling in parental plants could induce drought tolerance in the offspring is not known. In this study, drought priming was successively applied in the first, the second and the third generation of wheat to obtain the plants of T1 (primed for one generation), T2 (primed for two generations), T3 (primed for three generations). The differently primed plants were then subjected to drought stress during grain filling in the fourth generation. Under drought stress, the parentally primed (T1D, T2D, T3D) plants, disregarding the number of generations, showed higher grain yield, leaf photosynthetic rate and antioxidant capacity as well as lower [Formula: see text] release rate and contents of H2O2 and MDA than the non-primed (T0D) plants, suggesting that drought priming induced the transgenerational stress tolerance to drought stress. Moreover, the parentally primed plants showed higher leaf water status, which may result from the higher contents of proline and glycine betaine, and higher activities of ?1-pyrroline-5-carboxylate synthetase (P5CS) and betaine aldehyde dehydrogenase (BADH), compared with the non-primed plants under drought stress. In addition, there was no significant difference among three generations under drought, and the drought priming in parental generations did not affect the grain yield of the offspring plants under control condition. Collectively, the enhanced accumulation of proline and glycine betaine in the parentally primed plants could have played critical roles in parental priming induced tolerance to drought stress. This research provided a potential approach to improve drought tolerance of offspring plants by priming parental plants.

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Parental legacy in insects: variation of transgenerational immune priming during offspring development.

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