Shianiou Gavriella, Teloni Savvas, Apidianakis Yiorgos
Department of Biological Sciences, University of Cyprus, Nicosia 2109, Cyprus.
Metabolites. 2023 Feb 24;13(3):340. doi: 10.3390/metabo13030340.
A trade-off hypothesis pertains to the biased allocation of limited resources between two of the most important fitness traits, reproduction and survival to infection. This quid pro quo manifests itself within animals prioritizing their energetic needs according to genetic circuits balancing metabolism, germline activity and immune response. Key evidence supporting this hypothesis includes dipteran fecundity being compromised by systemic immunity, and female systemic immunity being compromised by mating. Here, we reveal a local trade-off taking place in the female midgut upon immune challenge. Genetic manipulation of intestinal motility, permeability, regeneration and three key midgut immune pathways provides evidence of an antagonism between specific aspects of intestinal defense and fecundity. That is, juvenile hormone (JH)-controlled egg laying, lipid droplet utilization and insulin receptor expression are specifically compromised by the immune deficiency (Imd) and the dual oxidase (Duox) signaling in the midgut epithelium. Moreover, antimicrobial peptide (AMP) expression under the control of the Imd pathway is inhibited upon mating and JH signaling in the midgut. Local JH signaling is further implicated in midgut dysplasia, inducing stem cell-like clusters and gut permeability. Thus, midgut JH signaling compromises host defense to infection by reducing Imd-controlled AMP expression and by inducing dysplasia, while midgut signaling through the Imd and Duox pathways compromises JH-guided metabolism and fecundity.
一种权衡假说涉及在繁殖和抗感染生存这两个最重要的适应性特征之间对有限资源的偏向性分配。这种交换在动物体内表现为，它们根据平衡新陈代谢、生殖系活动和免疫反应的遗传回路来优先满足自身的能量需求。支持这一假说的关键证据包括，全身免疫会损害双翅目昆虫的繁殖力，而交配会损害雌性的全身免疫。在此，我们揭示了雌性中肠在受到免疫挑战时会发生局部权衡。对肠道蠕动、通透性、再生以及三条关键的中肠免疫途径进行基因操作，为肠道防御的特定方面与繁殖力之间的拮抗作用提供了证据。也就是说，保幼激素（JH）控制的产卵、脂滴利用和胰岛素受体表达，会因中肠上皮细胞中的免疫缺陷（Imd）和双氧化酶（Duox）信号传导而受到特异性损害。此外，在交配和中肠中的JH信号传导作用下，Imd途径控制下的抗菌肽（AMP）表达会受到抑制。局部JH信号传导还与中肠发育异常有关，会诱导干细胞样簇的形成和肠道通透性增加。因此，中肠JH信号传导通过降低Imd控制的AMP表达以及诱导发育异常，损害宿主对感染的防御能力，而中肠通过Imd和Duox途径的信号传导则会损害JH引导的新陈代谢和繁殖力。
