The evolution of constitutively active humoral immune defenses in Drosophila populations under high parasite pressure
The evolution of constitutively active humoral immune defenses in Drosophila populations under high parasite pressure
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DOI：
10.1101/2023.10.02.560629
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发表时间：
2023-10
期刊：
影响因子：
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通讯作者：
Shuyu Olivia Zhou;Ramesh Arunkumar;S. Ding;Alexandre B. Leitão;F. Jiggins
中科院分区：
文献类型：
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作者：
Shuyu Olivia Zhou;Ramesh Arunkumar;S. Ding;Alexandre B. Leitão;F. Jiggins
宿主采用组成型和诱导型免疫机制来防御感染。组成免疫允许更快的响应，但它总是伴随着相关的成本。这种速度和健身成本之间的权衡导致的理论预测，组成性免疫将有利于寄生虫暴露频繁。我们选择了高寄生压力下的果蝇种群从寄生蜂Leptopilina boulardi。通过RNA测序，我们发现这些种群中抗性的演变与它们发展由幼虫脂肪体介导的组成性激活的体液免疫有关。此外，这些进化的种群也能够诱导基因表达以响应感染到更高的水平，这表明对寄生虫的体液免疫应答总体上更活跃。抗寄生虫免疫反应还依赖于感染后肌肉中激活的JAK/STAT信号通路，并且这种诱导的反应仅在高寄生虫压力下进化的种群中观察到。我们发现诱导这种JAK/STAT反应的细胞因子Upd 3由未成熟的板层细胞表达。此外，这些免疫细胞在群体进化出抗性时组成性存在，这可能解释了为什么它们获得了激活JAK/STAT信号传导的能力。因此，在强烈的寄生作用下，种群通过增加组成性免疫防御和诱导性免疫防御来进化出抵抗力，并且这两种形式的免疫之间可能存在相互作用。免疫防御可以在感染后诱导，或者它们可能是组成性活跃的，即使在未感染的个体中也是如此。由于组成性免疫是一种更快速的反应，理论预测，当动物经常遇到寄生虫时，它将受到青睐。当我们将黑腹果蝇种群置于其天然寄生虫Leptopilina boulardi寄生蜂的高寄生率下时，我们确实观察到免疫反应变得组成性活跃。未受感染的昆虫具有激活的体液免疫应答，并产生通常在感染后诱导的分泌精氨酸的免疫细胞。然而，我们也发现，这些人群进化出了更大的诱导反应。这包括感染后细胞因子反应大大增加，表明免疫系统某些方面的组成性激活可能允许在其他组织中产生更大的诱导反应。
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. Author Summary Immune defenses can be induced after infection or they may be constitutively active, even in uninfected individuals. As constitutive immunity is a more rapid response, theory predicts that it will be favored when animals frequently encounter parasites. When we subjected populations of Drosophila melanogaster to high rates of parasitization from its natural parasite, Leptopilina boulardi parasitoid wasps, we indeed observed that the immune response became constitutively active. Uninfected insects had an activated humoral immune response and produced cytokine-secreting immune cells that were normally induced after infection. However, we also found that these populations evolved a greater induced response. This included a greatly increased cytokine response after infection, suggesting that the constitutive activation of some aspects of the immune system may allow a greater induced response in other tissues.