Malnutrition is a global concern, and many populations are experiencing malnutrition for generations in many parts of the world. Restricted resource availability under malnutrition leads to impaired body metabolism, which in turn affects various life-history traits. It has been indicated that reduced immunity and therefore, susceptibility to infection is one major consequence of malnutrition. However, to date, it is unclear how it affects immunity & infection response in populations under chronic malnutrition. In this study, we have addressed this question using Drosophila melanogaster populations adapted against chronic malnutrition in the larval stages. To test that, we have used Providencia rettgeri infection both at pre-adult and adult life stages, followed by assessing their immune-competence and disease- transmission risk. This result aligns with the elevated pathogen clearance in maladapted larvae compared to controls. Moreover, we have identified that underpinning immune mechanisms attributed to insect cellular & humoral immunity, such as crystal cell number, Phenol oxidase activity, and consistently display an elevated level irrespective of identity (i.e., pathogen-infected vs. mock-infected) suggesting a basal increase of immune traits associated with larval-maladaptation. We furthermore evaluated the plausible ecological connection associated with larval maladaptation to adult traits upon infection using the same pathogen. As expected, here we identified a substantial fitness loss followed by elevated pathogen load across infection doses, suggesting an antagonistic pleiotropic response across Drosophila life stages. As the fitness loss indicates an immune-compromised body condition, we, therefore, continued to test the disease transmission risk of these evolved lines as an ecological approach. Surprisingly, here we have identified these larval-maladapted adults shedding a substantially more pathogen compared to controls while passaging through their body. The passaged pathogen through malnutrition lines also induced a significant fecundity loss compared to control counterparts while inhabiting a common uninfected fly line; WSO118, suggesting either (a) higher shedding or (b) increased virulence in passaged pathogen facilitates disease transmission risk to the surrounding susceptible population. Now to disentangle the effect of higher shedding or increased virulence we have adjusted to a fixed dose to control and maladapted passaged pathogens & introduced the secondary infection to a common host genotype, i.e., control flies. Surprisingly, here we have identified substantially higher mortality for maladapted-fly passaged pathogen compared to control passaged, suggesting that maladapted fly physiology facilitates enhanced virulence. To check whether such enhanced virulence shows consistency against other fly genotypes, we have used those passaged pathogens to infect other fly lines i.e., WSO118, Oregon R & the results remain the same as mentioned previously. Finally, the enhanced virulence in pathogen passaged through maladapted fly lines was confirmed by identifying different SNPs-related virulence factors' expression by whole genome sequencing. Taken together, this study suggests, that maladaptation leads to general stress response and is therefore beneficial against infection. However, that is restricted to certain life stages in fruit flies as it also facilitates disease transmission risk to uninfected individuals.
Chronic adaptation to malnutrition in the pre-adult stage mitigates infection costs at the expense of disease transmission risk in Drosophila adults: a novel trade-off in immunity.