Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect

Abstract

Summary1. When parasitized, both vertebrates and invertebrates can enhance the immune defence of their offspring, although this transfer of immunity is achieved by different mechanisms. In some insects, immune-challenged males can also initiate trans-generational immune priming (TGIP), but its expressions appear qualitatively different from the one induced by females similarly challenged. 2. The existence of male TGIP challenges the traditional view of the parental investment theory, which predicts that females should invest more into their progeny than males. However, sexual dimorphism in life-history strategies and the potential costs associated with TGIP may nevertheless lead to dissymmetric investment between males and females into the immune protection of the offspring. 3. Using the yellow mealworm beetle, Tenebrio molitor, we show that after parental exposure to a bacterial-like infection, maternal and paternal TGIP are associated with the enhancement of different immune effectors and different fitness costs in the offspring. While all the offspring produced by challenged mothers had enhanced immune defence, only those from early reproductive episodes were immune primed by challenged fathers. 4. Despite the fact that males and females may share a common interest in providing their offspring with an immune protection from the current pathogenic threat, they seem to have evolved different strategies concerning this investment.

Endogenous egg immune defenses in the yellow mealworm beetle (Tenebrio molitor)

“…This transgenerational immune priming (TGIP) increases immune activity in eggs laid by immune challenged parents, even in the absence of egg infection (Little and Kraaijeveld, 2004). Priming prepares the eggs for the impending danger by triggering differential expression of immune-related genes in eggs and/or via the direct transmission of immune factors into eggs (Freitak et al, 2014(Freitak et al, , 2009Knorr et al, 2015;Trauer-Kizilelma and Hilker, 2015;Trauer and Hilker, 2013;Zanchi et al, 2011).…”

Transgenerational interactions involving parental age and immune status affect female reproductive success inDrosophila melanogaster

“…We experimentally address the extent to which interactions between maternal and paternal age, and maternal, paternal and offspring immune activation, shape early-life reproductive success. By exploring the interaction between parental immune status and offspring immune status, we are also able to explore the potential for parental transfer of innate immunity factors, a controversial premise with emerging experimental support [9,[33][34][35][36]42,43].…”

“…In this adaptive branch, studies have demonstrated age-related deterioration caused by alterations of T cells and a decreasing abundance of naive B cells [25], as well as general transgenerational effects in which mothers transfer immune factors to offspring through the placenta, colostrum or breast milk [3,28]. Less is known about the capacity for age-dependent or transgenerational effects in the innate branch of the immune system common to all metazoans [9,[25][26][27][29][30][31]. Historically, it was assumed that the innate immune system only provided immediate, non-specific immune responses, lacking in immune memory [32] and transgenerational transfer of immune factors [33].…”

“…These effects can be mediated, for example, through transfer of nutrition via the egg, direct resource provisioning, protection against predators, or via the passive transfer of immune factors to offspring [1,3]. Recently, evidence has also accumulated that suggests sizeable contributions of non-genetic paternal effects to offspring fitness [4][5][6], such as, for example, the transfer of accessory gland proteins [4,7], epigenetic mechanisms [8] or via the transfer of immune factors [9]. However, compared with the wealth of studies exploring maternal effects, little is still known about the pervasiveness and magnitude of paternal effects, particularly in species that lack overt paternal care [6].…”

Sustainable farming of the mealworm Tenebrio molitor for the production of food and feed

“…Whereas immune priming increases host resistance to pathogens during second and subsequent encounters, transgenerational immune priming allows the offspring of the host to benefit from the same resistance even on their first encounter with the pathogen (Figure 3) [129][130][131][132][133]. However, individual immune priming by systemic injection would prove difficult in mass-reared insects due to their relatively small size and great number.…”