Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum

Abstract

Summary1. Parasitized females in mammals, fish and birds can enhance the immune defence of their offspring by transferring specific antibodies for the embryo. Likewise, social insect mothers transfer immunity despite the fact that invertebrates lack antibodies. 2. Female trans-generational immune priming is consistent with parental investment theory, because mothers invest more into rearing their offspring than fathers. However, when immune priming is not directly linked to parental care, as is often the case in insects that abandon their eggs after oviposition, both sexes might benefit from protecting their offspring. 3. Using the red flour beetle, Tribolium castaneum, we show that after parental exposure to heatkilled bacteria, trans-generational immune priming occurs through fathers as well as mothers. 4. This novel finding challenges the traditional view that males provide only genes to their offspring in species without paternal care, and raises the possibility of a division of tasks with respect to immune protection between parents.

The maternal transfer of bacteria can mediate trans-generational immune priming in insects

“…4,8 However, the maternal transfer of bacteria or bacterial fragments does not explain the paternal immune priming of offspring in the red flour beetle T. castaneum, suggesting other mechanisms can be involved in this phenomenon. 11,28 In contrast, we observed the highest levels of immunity-related gene expression in G. mellonella eggs from individuals that had fed as larvae on pathogenic S. entomophila. This discrepancy can be explained by the different effects of injected soluble microbial elicitors and orallyadministered bacterial pathogens on immunity-related transcriptional reprogramming, as shown in T. castaneum.…”

“…Maternal effects have been well documented in the context of trans-generational priming, and are thought to play a central role e.g., in the induction of offspring immunocompetence, but significant paternal effects have only been observed in a few studies. 11 Despite the increasing evidence for trans-generational immune priming in insects, the mechanism underlying the transfer of information from the parental generation to the offspring is unknown. The direct transfer of immune-related factors (e.g., lysozymes or antimicrobial peptides) in the cytoplasm of the egg has been proposed.…”

Evolution of transgenerational immunity in invertebrates

“…Our analyses showed that while the results obtained from TER studies are largely consistent with our theoretical predictions, the signal is much less clear for TEI studies. We believe that an integrative view of the transgenerational immune memory requires both approaches [17,18,21,62,63].…”

Benefits and costs of parental care

“…Recently it has been shown that parents of some invertebrates (mostly insects) may also transfer some specific immune factors to their offspring (Freitak et al 2009 and references therein). A novel study also challenges the long-held idea that fathers do not transmit immune information to their offspring: in the red flour beetle (Tribolium castaneum) offspring sired by males exposed to heat-killed bacteria were more resistant to a pathogen infection than offspring from non-exposed males (Roth et al 2010). Seminal substances, genomic imprinting and/or micro RNAs in the sperm could explain these findings (Roth et al 2010).…”