Natural selection has driven the recurrent loss of an immunity gene that protects
            <i>Drosophila</i>
            against a major natural parasite

Arunkumar, Ramesh; Zhou, Shuyu Olivia; Day, Jonathan P.; Bakare, Sherifat; Pitton, Simone; Zhang, Yexin; Hsing, Chi-Yun; O’Boyle, Sinead; Pascual-Gil, Juan; Clark, Belinda; Chandler, Rachael J.; Leitão, Alexandre B.; Jiggins, Francis M.

doi:10.1073/pnas.2211019120

Cited by 9 publications

(15 citation statements)

References 64 publications

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“…Furthermore, upregulated genes are known to have important functions. Wasp extract increased the expression of both Tep1 and Lectin-24a ( 35 ), which play a role in killing parasitoids, and IBIN , which affects blood sugar levels ( 33 ). However, it is possible that the duration of these responses or some other response that we did not measure may differ between natural infection and our experimental induction of the immune response.…”

Section: Discussionmentioning

confidence: 99%

Activation of immune defences against parasitoid wasps does not underlie the cost of infection

Leitão,

Geldman,

Jiggins

2023

Front. Immunol.

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Parasites reduce the fitness of their hosts, and different causes of this damage have fundamentally different consequences for the evolution of immune defences. Damage to the host may result from the parasite directly harming its host, often due to the production of virulence factors that manipulate host physiology. Alternatively, the host may be harmed by the activation of its own immune defences, as these can be energetically demanding or cause self-harm. A well-studied model of the cost of infection is Drosophila melanogaster and its common natural enemy, parasitoid wasps. Infected Drosophila larvae rely on humoral and cellular immune mechanisms to form a capsule around the parasitoid egg and kill it. Infection results in a developmental delay and reduced adult body size. To disentangle the effects of virulence factors and immune defences on these costs, we artificially activated anti-parasitoid immune defences in the absence of virulence factors. Despite immune activation triggering extensive differentiation and proliferation of immune cells together with hyperglycaemia, it did not result in a developmental delay or reduced body size. We conclude that the costs of infection do not result from these aspects of the immune response and may instead result from the parasite directly damaging the host.

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Section: Discussionmentioning

confidence: 99%

Activation of immune defences against parasitoid wasps does not underlie the cost of infection

Leitão,

Geldman,

Jiggins

2023

Front. Immunol.

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“…The posterior and anterior data were combined to generate a list of parasitismresponsive genes in the D. melanogaster larval fat body. The line used in this study is a promoter reporter line expressing a Venus fluorescence protein under the promoter of the lectin-24A gene, created using a line harboring an attP site on the X chromosome (BDSC # 24408) [20].…”

Section: Changes In Gene Expression Following Selection/infection Ana...mentioning

confidence: 99%

“…However, the role of humoral immune mechanisms in anti-parasitoid immunity is not well characterized. A few secreted immune effectors have been shown to be involved in this response, including thioester-containing proteins (TEPs), where their mammalian counterparts are complement factors involved in the complement cascade [ 19 ], a C-type lectin called lectin-24A shown to be crucial in the encapsulation response [ 20 ], and serine proteases which play key roles in the melanization reaction and Toll pathway activation [ 21 , 22 ].…”

Section: Introductionmentioning

confidence: 99%

The evolution of constitutively active humoral immune defenses in Drosophila populations under high parasite pressure

Zhou,

Arunkumar,

Irfan

et al. 2024

PLoS Pathog

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Both constitutive and inducible immune mechanisms are employed by hosts for defense against infection. Constitutive immunity allows for a faster response, but it comes with an associated cost that is always present. This trade-off between speed and fitness costs leads to the theoretical prediction that constitutive immunity will be favored where parasite exposure is frequent. We selected populations of Drosophila melanogaster under high parasite pressure from the parasitoid wasp Leptopilina boulardi. With RNA sequencing, we found the evolution of resistance in these populations was associated with them developing constitutively active humoral immunity, mediated by the larval fat body. Furthermore, these evolved populations were also able to induce gene expression in response to infection to a greater level, which indicates an overall more activated humoral immune response to parasitization. The anti-parasitoid immune response also relies on the JAK/STAT signaling pathway being activated in muscles following infection, and this induced response was only seen in populations that had evolved under high parasite pressure. We found that the cytokine Upd3, which induces this JAK/STAT response, is being expressed by immature lamellocytes. Furthermore, these immune cells became constitutively present when populations evolved resistance, potentially explaining why they gained the ability to activate JAK/STAT signaling. Thus, under intense parasitism, populations evolved resistance by increasing both constitutive and induced immune defenses, and there is likely an interplay between these two forms of immunity.

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“…Based on these studies, here we investigated the regulation of Drosophila humoral antiparasitoid immunity mediated by the larval fat body. We focused on the lectin-24A gene, a key humoral immune effector in this response [12], and studied its induction with parasitization to understand the regulation of anti-parasitoid humoral immune mechanisms more broadly.…”

Section: Introductionmentioning

confidence: 99%

A humoral immune response to parasitoid wasps inDrosophilais regulated by JAK/STAT, NF-κB and GATA

Zhou,

Day,

Deplancke

et al. 2024

Preprint

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The two arms of innate immunity consist of the cell-mediated cellular defenses and the systemic humoral immune responses.Drosophilahumoral immune defenses in the context of antimicrobial immunity, particularly the regulation and activation of antimicrobial peptide secretion from the fat body, have been studied extensively. HowDrosophilaregulates humoral immunity against another major natural enemy, the parasitoid wasp, is less well-characterized. In this study, we focused on a gene crucial in anti-parasitoid immunity,lectin-24A, which is specifically induced following parasitization. We found that a fluorescent reporter driven by the region upstream oflectin-24Ashowed localized posterior expression in the larval fat body, theDrosophilatissue mediating humoral immunity. Furthermore, with RNA sequencing of the anterior and posterior fat body sections, we found that components of JAK/STAT, GATA, and Toll pathways were regulated differentially in the anterior-posterior axis of the fat body and/or by infection. Predicted binding motifs for transcription factors in all three of these pathways were identified in the 444bp upstream region of thelectin-24Agene, where scrambling these motifs leads to reduced basal or induced expression of the fluorescent reporter. Investigating each of these pathways, we found that JAK/STAT, the GATA factor Pannier, and the NF-κB factor dorsal all modulate the expression oflectin-24A. The binding motifs associated with these transcription factors were also enriched in the upstream sequences of parasitism-induced genes in the fat body. Taken together, these results indicate that JAK/STAT, Pannier, and NF-κB signaling are involved in the regulation oflectin-24Aand, more generally,Drosophilahumoral anti-parasitoid immunity after infection.

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Natural selection has driven the recurrent loss of an immunity gene that protects Drosophila against a major natural parasite

Cited by 9 publications

References 64 publications

Activation of immune defences against parasitoid wasps does not underlie the cost of infection

Activation of immune defences against parasitoid wasps does not underlie the cost of infection

The evolution of constitutively active humoral immune defenses in Drosophila populations under high parasite pressure

A humoral immune response to parasitoid wasps inDrosophilais regulated by JAK/STAT, NF-κB and GATA

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