The effect of diet and time after bacterial infection on fecundity, resistance, and tolerance in Drosophila melanogaster

Abstract

Mounting and maintaining an effective immune response in the face of infection can be costly. The outcome of infection depends on two host immune strategies: resistance and tolerance. Resistance limits pathogen load, while tolerance reduces the fitness impact of an infection. While resistance strategies are well studied, tolerance has received less attention, but is now considered to play a vital role in host–pathogen interactions in animals. A major challenge in ecoimmunology is to understand how some hosts maintain their fitness when infected while others succumb to infection, as well as how extrinsic, environmental factors, such as diet, affect defense. We tested whether dietary restriction through yeast (protein) limitation affects resistance, tolerance, and fecundity in Drosophila melanogaster. We predicted that protein restriction would reveal costs of infection. Because infectious diseases are not always lethal, we tested resistance and tolerance using two bacteria with low lethality: Escherichia coli and Lactococcus lactis. We then assayed fecundity and characterized bacterial infection pathology in individual flies at two acute phase time points after infection. As expected, our four fecundity measures all showed a negative effect of a low‐protein diet, but contrary to predictions, diet did not affect resistance to either bacteria species. We found evidence for diet‐induced and time‐dependent variation in host tolerance to E. coli, but not to L. lactis. Furthermore, the two bacteria species exhibited remarkably different infection profiles, and persisted within the flies for at least 7 days postinfection. Our results show that acute phase infections do not necessarily lead to fecundity costs despite high bacterial loads. The influence of intrinsic variables such as genotype are the prevailing factors that have been studied in relation to variation in host tolerance, but here we show that extrinsic factors should also be considered for their role in influencing tolerance strategies.

Genotype and diet affect resistance, survival, and fecundity but not fecundity tolerance

“…We used ten wild‐type populations. The locally collected population used in this study (1_4WS; Kutzer & Armitage, ) was maintained in a population cage with overlapping generations. Nine populations with variable fecundity (Ral208, Ral350, Ral367, Ral373, Ral375, Ral379, Ral406, Ral509 and Ral765) from the Drosophila Genetic Reference Panel (DGRP) originating from North Carolina, USA (Mackay et al ., ), were maintained in vials and placed onto new food every 2 weeks.…”

“…Aliquots of L. lactis and P. entomophila were stored in 34.4% glycerol at −80 °C. Lactococcus lactis was plated on lysogeny broth (LB) agar and P. entomophila was plated on LB agar containing 1% milk to select for protease positive clones (Neyen et al ., ), after which, bacterial preparation and infections were carried out following Kutzer & Armitage () using a randomized block design of 60 total treatment groups (10 genotypes × 2 diets × 3 infection treatments). In each experimental replicate, we processed three flies per treatment group, giving 21 flies per genotype × diet × infection treatment, that is 1260 flies in total.…”

“…The percent change for each individual was therefore calculated as ((individual infected fecundity ω i – mean Ringer's group fecundity ω 0 ) / ω 0 ) × 100. For statistical reasons, we standardized the change in fitness in this way to make the fecundity values more comparable across the two dietary treatments (Kutzer & Armitage, ).…”

“…Råberg et al ., ; Blanchet et al ., ; Sternberg et al ., ; Howick & Lazzaro, ; Parker et al ., ). It can also be a plastic response, where its expression is determined by the host environment, for example by the concentration of dietary glucose (Howick & Lazzaro, ) or yeast (Kutzer & Armitage, ). Therefore, variation in defence strategies within and between populations can be attributed to genetic (G) and environmental (E) factors or a combination of both (i.e.…”

Macronutrients modulate survival to infection and immunity in Drosophila

“…‘resistance’), it provided the host with the ability to reduce the damage of the infection on its health, also called ‘tolerance’ (Ayres & Schneider, , ). Diet composition may affect tolerance of infection (Howick & Lazzaro, ; Kutzer & Armitage, ; Miller & Cotter, ); for example, it has been shown that yeast restriction in Drosophila flies affects tolerance specifically to one strain of bacterium in a time‐dependent manner; however, no effect on resistance was detected (Kutzer & Armitage, ).…”