Trade‐offs between transgenerational transfer of nutritional stress tolerance and immune priming

Abstract

Summary1. Transgenerational effects are often assumed to have adaptive value as a driver of variation in offspring and parental fitness. Studies of transgenerational effects often focus on single environmental variables. However, in nature, it is unlikely for one factor to vary independently from others and there are likely to be trade-offs between different stressors. 2. We altered the nutritional environment of both parents and offspring to examine how nutritional stress influences transgenerational immune priming (TGIP) with a sublethal challenge by the bacterial pathogen Bacillus thuringiensis, in the cabbage looper, Trichoplusia ni. 3. Transgenerational immune priming was adaptive when offspring encountered the same pathogen experienced by their parents, such that offspring resistance to B. thuringiensis increased 1Á5-fold and antibacterial activity in the haemolymph increased by as much as 4-fold. However, this was not a general increase in pathogen resistance as susceptibility to a second pathogen, the baculovirus, TnSNPV remained the same. Interestingly, nutritional stress in the parents both enhanced nutritional stress tolerance of offspring and heightened resistance to both B. thuringiensis and TnSNPV. Elevated pathogen resistance was linked to increased egg size. 4. There was a significant trade-off between TGIP and the transfer of nutritional stress tolerance when parents encountered both stressors simultaneously, such that parents transferred resistance to pathogens but not nutritional stress tolerance. 5. These results highlight the trade-offs that can modulate the occurrence and magnitude of transgenerational effects and illustrate the importance of assessing interactions between multiple environmental variables. At high population densities, disease risk increases and resources become depleted. Thus, our findings could have significant implications for population dynamics.

Impact of non‐pathogenic bacteria on insect disease resistance: importance of ecological context

“…Thus, the use of two different classes of bacteria may have elicited a stronger response. Furthermore, while haemolymph immunity can play a role in insect resistance to Bt (Dubovskiy et al, 2008;Grizanova et al, 2014;Shikano et al, 2015), the concentration-dependent change in Bt-resistance of Pseudomonas-fed T. ni found here may have resulted from an altered composition of the midgut bacterial community. Direct antagonism of Bt by midgut bacteria, as observed in other lepidopteran larvae (Johnston & Crickmore, 2009;Raymond et al, 2010), might contribute to heightened resistance at low concentrations, whereas opportunistic invasion of the haemocoel by Pseudomonas spp.…”

“…Regardless of the mechanisms, slower growth from consuming non-entomopathogenic bacteria can be detrimental as it prolongs the exposure of the most vulnerable younger stages to pathogens and other natural enemies. Reduced food quality and the abundance of midgut bacteria are also associated with higher larval susceptibility to baculoviruses (Jakubowska et al, 2013;Shikano et al, 2015), and may have contributed to the slightly faster mortality of Pseudomonas-fed T. ni after virus challenge.…”

“…The lytic zone of inhibition was used to assess antibacterial activity as described in Shikano et al (2015).…”

“…We followed the protocol by Shikano et al (2015). Five microlitres of haemolymph were mixed with 100 μl of ice-cold phosphate-buffered saline (PBS) (pH 7.4).…”

Phylloplane bacteria increase the negative impact of food limitation on insect fitness

“…Egg provisioning or neonate size can relate to fitness of insects in terms of individual quality/vigour (Wellington, 1960) or to overwintering survival of embryonic larvae within eggs (Harvey, 1985;Fitzpatrick & Troubridge, 1993;Fischer et al, 2003). In addition, a recent study has also shown increased egg size of cabbage looper, T. ni, after larvae were exposed to a sub-lethal concentration of the bacterial pathogen Bacillus thuringiensis (Shikano et al, 2015a). We predicted that egg size would increase for females fed induced foliage or foliar bacteria, if these acted as stressors that initiated higher investment in offspring quality versus quantity.…”