Experimental evolution of insect immune memory versus pathogen resistance

Abstract

Under strong pathogen pressure, insects often evolve resistance to infection. Many insects are also protected via immune memory (immune priming), whereby sublethal exposure to a pathogen enhances survival after secondary infection. Theory predicts that immune memory should evolve when the pathogen is highly virulent, or when pathogen exposure is relatively rare. However, there are no empirical tests of these hypotheses, and the adaptive benefits of immune memory relative to direct resistance against a pathogen are poorly understood. To determine the selective pressures and ecological conditions that shape immune evolution, we imposed strong pathogen selection on flour beetle () populations, infecting them with (Bt) for 11 generations. Populations injected first with heat-killed and then live Bt evolved high basal resistance against multiple Bt strains. By contrast, populations injected only with a high dose of live Bt evolved a less effective but strain-specific priming response. Control populations injected with heat-killed Bt did not evolve priming; and in the ancestor, priming was effective only against a low Bt dose. Intriguingly, one replicate population first evolved priming and subsequently evolved basal resistance, suggesting the potential for dynamic evolution of different immune strategies. Our work is the first report showing that pathogens can select for rapid modulation of insect priming ability, allowing hosts to evolve divergent immune strategies (generalized resistance versus specific immune memory) with potentially distinct mechanisms.

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

“…Together, these results indicate that pathogen-mediated reduction in life span may impose strong selection for a priming response in natural populations, as predicted by theoretical models (Best et al, 2013) and observed in laboratory-evolved populations (Khan et al, 2017). Second, we found a life stage-specific negative relationship (a possible trade-off) with early reproductive success (measured over 2 days) that may constrain the strength of priming in adults, but not in larvae.…”

“…Prior studies also show that priming alters bacterial load, though the timing (Tate, Andolfatto, Demuth, & Graham, ) and direction of the impact varies (compare Pham, Dionne, Shirasu‐hiza, & Schneider, ; Kutzer, Kurtz, & Armitage, ). Together, these results indicate that pathogen‐mediated reduction in life span may impose strong selection for a priming response in natural populations, as predicted by theoretical models (Best et al, ) and observed in laboratory‐evolved populations (Khan et al, ). Second, we found a life stage‐specific negative relationship (a possible trade‐off) with early reproductive success (measured over 2 days) that may constrain the strength of priming in adults, but not in larvae.…”

“…We note that pricking alone can lead to wounding that can activate non‐specific immune responses (Behrens et al, ). Yet, we think that this is insufficient to provide survival benefits of priming since other experiments with laboratory‐adapted outbred populations (described in Khan et al, ) suggest that naïve beetles or beetles injected with Ringer solution are equally susceptible to live infection later in life (see Figure S1). However, we did not test whether such wounding affects other traits such as reproduction, immune components or development.…”

“…DSM 2046, originally isolated from a Mediterranean flour moth) to measure within-generation priming for all populations as described in Khan et al (2016a). Our previous experiments show that flour beetles produce priming responses that are highly specific to the strain of B. thuringiensis (Bt) used in this study (Khan et al, 2017). Briefly, we pricked adults between the head and thorax, and larvae between the last and last but one segment, using a 0.1-mm insect pin (FST, CA) dipped in heat-killed bacterial slurry (i.e.…”

“…In insects, encapsulation ability increases with the virulence of the pathogen (Kraaijeveld & Van Alphen, 1994), and natural populations of Drosophila melanogaster exposed to diverse pathogen communities show an increased ability to clear bacterial infection (Corby-Harris & Promislow, 2008). Strong pathogen selection may similarly play a direct role in the evolution of the insect priming response (Best, Tidbury, White, & Boots, 2013), as we recently demonstrated: immune priming evolved rapidly in laboratory-selected flour beetle populations exposed to a lethal dose of bacterial infection (Khan, Prakash, & Agashe, 2017). Does strong pathogen pressure also select for priming in natural conditions?…”