Abstract

In many vertebrates and invertebrates, offspring whose mothers have been exposed to pathogens can exhibit increased levels of immune activity and/or increased survival to infection. Such phenomena, called “Trans-generational immune priming” (TGIP) are expected to provide immune protection to the offspring. As the offspring and their mother may share the same environment, and consequently similar microbial threats, we expect the immune molecules present in the progeny to be specific to the microbes that immune challenged the mother. We provide evidence in the mealworm beetle Tenebrio molitor that the antimicrobial activity found in the eggs is only active against Gram-positive bacteria, even when females were exposed to Gram-negative bacteria or fungi. Fungi were weak inducers of TGIP while we obtained similar levels of anti-Gram-positive activity using different bacteria for the maternal challenge. Furthermore, we have identified an antibacterial peptide from the defensin family, the tenecin 1, which spectrum of activity is exclusively directed toward Gram-positive bacteria as potential contributor to this antimicrobial activity. We conclude that maternal transfer of antimicrobial activity in the eggs of T. molitor might have evolved from persistent Gram-positive bacterial pathogens between insect generations.

Highlights

  • Maternal effects are of paramount importance for offspring fitness when mothers adjust the phenotype of their offspring to match the environment that they are likely to experience [1]

  • We found that enhanced levels of antimicrobial activity in the eggs of immune challenged females of the mealworm beetle, Tenebrio molitor, were only active against Gram-positive bacteria, whatever the microorganism used for the maternal challenge

  • These results suggest that maternal transfer of antimicrobial activity in the eggs in T. molitor might have evolved from the persistence of Gram-positive bacterial pathogens between insect generations

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Summary

Introduction

Maternal effects are of paramount importance for offspring fitness when mothers adjust the phenotype of their offspring to match the environment that they are likely to experience [1]. In many different groups of animals, the immunogenic experience of the mother is transferred to otherwise “naïve” offspring and can protect it against infection [2, 3]. Maternal transfer of immunity has been well studied in vertebrates, in which infected females can transfer specific antibodies to the offspring via the placenta and milk in mammals during lactation, or via the egg yolk in birds, reptiles and fish [3, 4]. Invertebrates lack the antibodies that vertebrate females transfer to their offspring. Maternal transfer of immunity, referred as trans-generational immune priming (TGIP), occurs in invertebrates too [5], suggesting that it has to be achieved by other, yet unknown, mechanisms. The effects of TGIP have been revealed through enhanced levels of immune activity and/or an increased survival to infection in primed offspring. The immune protection provided to the offspring can exhibit variable levels of specificity

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