Abstract
Natural selection should favor the transfer of immune competence from one generation to the next in a context-dependent manner. Transgenerational immune priming (TGIP) is expected to evolve when species exploit pathogen-rich environments and exhibit extended overlap of parent–offspring generations. Dampwood termites are hemimetabolous, eusocial insects (Blattodea: Archeotermopsidae) that possess both of these traits. We predict that offspring of pathogen-exposed queens of Zootermopsis angusticollis will show evidence of a primed immune system relative to the offspring of unexposed controls. We found that Relish transcripts, one of two immune marker loci tested, were enhanced in two-day-old embryos when laid by Serratia-injected queens. These data implicate the immune deficiency (IMD) signaling pathway in TGIP. Although an independent antibacterial assay revealed that embryos do express antibacterial properties, these do not vary as a function of parental treatment. Taken together, Z. angusticollis shows transcriptional but not translational evidence for TGIP. This apparent incongruence between the transcriptional and antimicrobial response from termites suggests that effectors are either absent in two-day-old embryos or their activity is too subtle to detect with our antibacterial assay. In total, we provide the first suggestive evidence of transgenerational immune priming in a termite.
Highlights
Mendelian genetics have dominated our perception of the laws of inheritance: the progeny’s phenotype is shaped by instructions inherited from the parental DNA
Our data indicate that offspring of Serratia-infected queens have a significantly greater abundance of Relish transcripts compared to embryos of saline queens (Figure 2A)
Regardless of whether transcripts are of maternal or embryonic origin, we showed that the transcription of at least one immune gene (Relish) at this early stage of ontogeny is influenced by maternal pathogenic stress and is indicative of Transgenerational immune priming (TGIP)
Summary
Mendelian genetics have dominated our perception of the laws of inheritance: the progeny’s phenotype is shaped by instructions inherited from the parental DNA. Within the past ~20 years, a fundamental shift in our understanding of heritable phenotypes has taken place—namely, that some environmentally acquired information may be transferred between generations, from parent to offspring and even across subsequent generations. Such context-dependent inheritance does not involve nucleotide changes in the genetic code [1,2,3]. The parental transfer of nutrients, hormones, cytoplasmic factors, small RNAs and other information-bearing molecules, as well as epigenetic tags that can modulate offspring gene expression [4,5,6], results in changes to offspring phenotype that anticipate environmental challenges and their demands. Through parental effects (both maternal and paternal across one generation [11]) or transgenerational effects (across multiple generations [1,2,3,12,13]), parents can convey environmentally acquired qualities to their offspring, thereby anticipating their offspring’s fit to their environment [2,12,13]
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