Environmental temperature variation influences fitness trade-offs and tolerance in a fish-tapeworm association

Background Increasing temperatures are predicted to strongly impact host-parasite interactions, but empirical tests are rare. Host species that are naturally exposed to a broad temperature spectrum offer the possibility to investigate the effects of elevated temperatures on hosts and parasites. Using three-spined sticklebacks, Gasterosteus aculeatus L., and tapeworms, Schistocephalus solidus (Müller, 1776), originating from a cold and a warm water site of a volcanic lake, we subjected sympatric and allopatric host-parasite combinations to cold and warm conditions in a fully crossed design. We predicted that warm temperatures would promote the development of the parasites, while the hosts might benefit from cooler temperatures. We further expected adaptations to the local temperature and mutual adaptations of local host-parasite pairs. Results Overall, S. solidus parasites grew faster at warm temperatures and stickleback hosts at cold temperatures. On a finer scale, we observed that parasites were able to exploit their hosts more efficiently at the parasite’s temperature of origin. In contrast, host tolerance towards parasite infection was higher when sticklebacks were infected with parasites at the parasite’s ‘foreign’ temperature. Cold-origin sticklebacks tended to grow faster and parasite infection induced a stronger immune response. Conclusions Our results suggest that increasing environmental temperatures promote the parasite rather than the host and that host tolerance is dependent on the interaction between parasite infection and temperature. Sticklebacks might use tolerance mechanisms towards parasite infection in combination with their high plasticity towards temperature changes to cope with increasing parasite infection pressures and rising temperatures

Female-limited X chromosome evolution reveals that lifespan is mainly modulated by interlocus rather than intralocus sexual conflict

Sexual dimorphism in somatic investment may be shaped by two distinct forms of sexual conflict; under intralocus sexual conflict (IASC), males and females have different optimal levels of somatic investment but are constrained from reaching their respective optima by their shared genome, while under interlocus sexual conflict (IRSC), males and females have different optimal sexual strategies, which could have direct or indirect effects on levels of somatic investment. We investigated effects of IASC and IRSC on two aspects of somatic investment, immune defence strategies and longevity, using previously established female-limited experimental evolution lines in Drosophila melanogaster. We found little evidence for any effect of either type of sexual conflict on investment in the immune defence resistance or tolerance. Nor did we find convincing evidence that longevity is subject to IASC in this species. However, we did find evidence that increased female control over mating rate had important and opposite effects on longevity between the sexes. Specifically, females that had adapted to high levels of female control over mating had a longer lifespan when kept in mixed-sex groups, while males had shorter longevity, perhaps due to increased investment in post-copulatory sexual selection. These novel results show that female control over mating rates may have important and unexpected effects on patterns of somatic investment

Data from: Specificity of oral immune priming in the red flour beetle Tribolium castaneum

Immune specificity is the degree to which a host’s immune system discriminates among various pathogens or antigenic variants. Vertebrate immune memory is highly specific due to antibody responses. On the other hand, some invertebrates show immune priming, i.e. improved survival after secondary exposure to a previously encountered pathogen. Until now, specificity of priming has only been demonstrated via the septic infection route or when live pathogens were used for priming. Therefore, we tested for specificity in the oral priming route in the red flour beetle, Tribolium castaneum. For priming, we used pathogen-free supernatants derived from three different strains of the entomopathogen, Bacillus thuringiensis, which express different Cry toxin variants known for their toxicity against this beetle. Subsequent exposure to the infective spores showed that oral priming was specific for two naturally occurring strains, while a third engineered strain did not induce any priming effect. Our data demonstrate that oral immune priming with a non-infectious bacterial agent can be specific, but the priming effect is not universal across all bacterial strains

Model 4a, Fig. 4a

Data corresponding to Model 4a, Figure 4a and Table 3

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

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

Fig. S3

Survival data corresponding to Fig. S3

Fig. S1, S2 & Appendix S1

Data corresponding to Figures S1 & S2 and mating data in Appendix S1

Kutzer et al data files

Data files are labelled according to the experiment and model number(s). Full details on the statistical models and model numbers can be found in Appendix 1, which is a supplementary file for the paper

Model 4b, Fig. 4b

Data corresponding to Model 4b, Figure 4b and Table

Model 5, Fig. 5

Data corresponding to Model 5, Figure 5 and Table 4