Pathogen susceptibility and fitness costs explain variation in immune priming across natural populations of flour beetles

Abstract

In many insects, individuals primed with low doses of pathogens early in life have higher survival after exposure to the same pathogen later in life. Yet, our understanding of the evolutionary and ecological history of priming of immune response in natural insect populations is limited. Previous work demonstrated population‐, sex‐ and stage‐specific variation in the survival benefit of priming response in flour beetles (Tribolium castaneum) infected with their natural pathogen Bacillus thuringiensis. However, the evolutionary forces responsible for this natural variation remained unclear. In the present work, we tested whether the strength of the priming response (measured as the survival benefit after priming and subsequent infection, relative to unprimed controls) was associated with multiple fitness parameters and immune components across 10 flour beetle populations collected from different locations in India. Our results suggest two major selective pressures that may explain the observed inter‐population variation in priming: (a) Basal pathogen susceptibility – populations that were more susceptible to infection produced a stronger priming response, and (b) Short‐term early reproductive success – populations where primed females produced more offspring early in life (measured over 2 days) had lower survival benefit (measured over 120 days), suggesting a potential trade‐off between early reproduction and priming response. However, the negative association between survival and reproduction is limited to priming and infection in adults, but not in larvae. While other components of beetle fitness (starvation resistance and larval development) and immune function (haemolymph antibacterial activity and antimicrobial quinone secretion) also varied widely across populations, none of them was correlated with the variation in priming responses across populations. Our work is the first systematic empirical demonstration of multiple selective pressures that may govern the evolution of immune priming in the wild. We hope that this motivates further experiments to establish the role of pathogen‐imposed selection and fitness costs in the evolution of priming in natural insect populations.

The Costs and Benefits of Basal Infection Resistance vs Diverse Immune Priming Responses in an Insect

“…For instance, mounting a within-generation priming response helped no_evol_C beetles to increase their reproduction after infection; whereas infected evol_priming_I beetles, despite evolving survival benefits, could not improve their reproduction. These results mirror our recent observations with wild-caught populations, where primed and infected females with increased post-infection lifespan produced fewer offspring (Khan et al, 2019) and vice versa. We thus speculate that a hidden trade-off with post-infection reproduction might constrain the survival benefits of within-generation priming responses at a much lower level than resistance (see Fig.…”

“…In general, costs of pathogen resistance may manifest as widespread tradeoffs with other life-history parameters as well, including reproduction (Reviewed in Sheldon and Verhulst, 1996; Lochmiller and Deerenberg, 2000; Rolff and Siva-Jothy, 2003; Schwenke et al, 2016). In contrast, the impact of immune priming-mediated protection on various fitness parameters has only recently been tested: e.g., primed mosquitoes (Contreras-Garduño et al, 2014), tobacco hornworms (Trauer and Hilker, 2013) and flour beetles (Khan et al, 2019) show reduced fecundity or primed mealworm beetle mothers produced progeny that developed slowly (Zanchi et al, 2011). Although these experiments revealed diverse fitness impacts of mounting priming responses using phenotypic manipulations, the actual costs of evolving, maintaining and deploying priming responses in populations while facing persistent pathogen-imposed selection have never been measured in detail (also see Ferro et al, 2019).…”

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

“…To measure evolved vulnerability to a bacterial pathogen, we first isolated 2-day-old experimental virgin females from each of the lines and paired them individually with a single male from their own line for 5 h. Simultaneously, we also collected another subset of females that were held as virgin throughout the experiment. On day 3 post eclosion, we infected females with a strain (DSM 2046) of the entomopathogenic gram-positive bacteria Bacillus thuringiensis, described in [ 130 ]. Beetles were first anaesthetized with carbon-dioxide and then pricked at the lateral side of the lower abdomen, using a 0.1-mm minutien pin (Fine Science Tools) dipped in overnight bacterial suspension of 1 OD or 2 OD (subcultured from an overnight culture of the bacteria).…”

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

“…Simultaneously, we also collected another subset of females that were held as virgin throughout the experiment. On day three post eclosion, we infected females with a strain (DSM 2046) of the entomopathogenic gram-positive bacteria Bacillus thuringiensis, described in (130). Beetles were first anesthetized with carbon-dioxide and then pricked at the lateral side of the lower abdomen, using a 0.1mm minutien pin (Fine Science Tools) dipped in overnight bacterial suspension of 1 OD or 2 OD (subcultured from an overnight culture of the bacteria).…”