IMD-mediated innate immune priming increases Drosophila survival and reduces pathogen transmission

Prakash, Arun; Fenner, Florence; Shit, Biswajit; Salminen, Tiina S.; Monteith, Katy M.; Khan, Imroze; Vale, Pedro F.

doi:10.1371/journal.ppat.1012308

Cited by 5 publications

References 84 publications

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Genetic Variation in Trophic Avoidance Behaviour Shows Fruit Flies are Generally Attracted to Bacterial Substrates

Monteith,

Thornhill,

Vale

2024

Ecology and Evolution

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Pathogen avoidance behaviours are often assumed to be an adaptive host defence. However, there is limited experimental data on heritable, intrapopulation phenotypic variation for avoidance, a strong prerequisite for adaptive responses to selection. We investigated trophic pathogen avoidance in 122 inbred Drosophila melanogaster lines, and in a derived outbred population. Using the FlyPAD system, we tracked the feeding choice that flies made between substrates that were either clean or contained a bacterial pathogen. We uncovered significant, but weakly heritable variation in the preference index amongst fly lines. However, instead of avoidance, most lines demonstrated a preference for substrates containing several bacterial pathogens, showing avoidance only for extremely high bacterial concentrations. Bacterial preference was not associated with susceptibility to infection and was retained in flies with disrupted immune signalling. Phenotype–genotype association analysis indicated several novel genes (CG2321, CG2006, and ptp99A) associated with increased preference for the bacterial substrate, while the amino‐acid transporter sobremesa was associated with greater aversion. Given the known fitness benefits of consuming high‐protein diets, our results suggest that bacterial attraction may instead reflect a dietary preference for protein over carbohydrate. More work quantifying intrapopulation variation in avoidance behaviours is needed to fully assess its importance in host–pathogen evolutionary ecology.

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Genetic Variation in Trophic Avoidance Behaviour Shows Fruit Flies are Generally Attracted to Bacterial Substrates

Monteith,

Thornhill,

Vale

2024

Ecology and Evolution

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Mitochondrial background can explain variable costs of immune deployment

Kutzer,

Cornish,

Jamieson

et al. 2024

Journal of Evolutionary Biology

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Organismal health and survival depend on the ability to mount an effective immune response against infection. Yet immune defence may be energy-demanding, resulting in fitness costs if investment in immune function deprives other physiological processes of resources. While evidence of costly immunity resulting in reduced longevity and reproduction is common, the role of energy-producing mitochondria on the magnitude of these costs is unknown. Here, we employed Drosophila melanogaster cybrid lines, where several mitochondrial genotypes (mitotypes) were introgressed onto a single nuclear genetic background, to explicitly test the role of mitochondrial variation on the costs of immune stimulation. We exposed female flies carrying one of nine distinct mitotypes to either a benign, heat-killed bacterial pathogen (stimulating immune deployment while avoiding pathology) or to a sterile control and measured lifespan, fecundity, and locomotor activity. We observed mitotype-specific costs of immune stimulation and identified a positive genetic correlation in immune-stimulated flies between lifespan and the proportion of time cybrids spent moving while alive. Our results suggests that costs of immunity are highly variable depending on the mitochondrial genome, adding to a growing body of work highlighting the important role of mitochondrial variation in host–pathogen interactions.

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Experimental evolution of a pathogen confronted with innate immune memory increases variation in virulence

Korša,

Baur,

Schulz

et al. 2024

Preprint

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Understanding the drivers and mechanisms of virulence evolution is still a major goal of evolutionary biologists and epidemiologists. Theory predicts that the way virulence evolves depends on the balance between the benefits and costs it provides to pathogen fitness. Additionally, host responses to infections, such as resistance or tolerance, play a critical role in shaping virulence evolution. But, while the evolution of pathogens has been traditionally studied under the selection pressure of host adaptive immunity, less is known about their evolution when confronted to simpler and less effective forms of immunity such as immune priming. In this study, we used a well-established insect model for immune priming – red flour beetles and their bacterial pathogen Bacillus thuringiensistenebrionis – to test whether this form of innate immune memory favors the evolution of higher virulence. Through controlled experimental evolution of the pathogen in primed versus non-primed hosts, we found no change in average virulence after eight selection cycles in primed host. However, we found a significant increase in the variation of virulence (i.e., host-killing ability) among independent pathogen lines evolved in primed host, and bacteria were unable to evolve resistance against host priming. Whole genome sequencing revealed increased activity in the bacterial mobilome (prophages and plasmids). Expression of the Cry toxin – a well-known virulence factor – was linked to evolved differences in copy number variation of the cry-carrying plasmid, though this did not correlate directly with virulence. These findings highlight that innate immune memory can drive variability in pathogen traits, which may favor adaptation to variable environments. This underscores the need to consider pathogen evolution in response to innate immune memory when applying these mechanisms in medicine, aquaculture, pest control, and insect mass production.

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IMD-mediated innate immune priming increases Drosophila survival and reduces pathogen transmission

Cited by 5 publications

References 84 publications

Genetic Variation in Trophic Avoidance Behaviour Shows Fruit Flies are Generally Attracted to Bacterial Substrates

Genetic Variation in Trophic Avoidance Behaviour Shows Fruit Flies are Generally Attracted to Bacterial Substrates

Mitochondrial background can explain variable costs of immune deployment

Experimental evolution of a pathogen confronted with innate immune memory increases variation in virulence

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