Hanson Mark A, Hamilton Phineas T, Perlman Steve J
Department of Biology, University of Victoria, Victoria, BC, Canada.
Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research, Toronto, Ontario, Canada.
BMC Evol Biol. 2016 Oct 24;16(1):228. doi: 10.1186/s12862-016-0805-y.
Drosophila is an important model for studying the evolution of animal immunity, due to the powerful genetic tools developed for D. melanogaster. However, Drosophila is an incredibly speciose lineage with a wide range of ecologies, natural histories, and diverse natural enemies. Surprisingly little functional work has been done on immune systems of species other than D. melanogaster. In this study, we examine the evolution of immune genes in the speciose subgenus Drosophila, which diverged from the subgenus Sophophora (that includes D. melanogaster) approximately 25-40 Mya. We focus on D. neotestacea, a woodland species used to study interactions between insects and parasitic nematodes, and combine recent transcriptomic data with infection experiments to elucidate aspects of host immunity.
We found that the vast majority of genes involved in the D. melanogaster immune response are conserved in D. neotestacea, with a few interesting exceptions, particularly in antimicrobial peptides (AMPs); until recently, AMPs were not thought to evolve rapidly in Drosophila. Unexpectedly, we found a distinct diptericin in subgenus Drosophila flies that appears to have evolved under diversifying (positive) selection. We also describe the presence of the AMP drosocin, which was previously thought to be restricted to the subgenus Sophophora, in the subgenus Drosophila. We challenged two subgenus Drosophila species, D. neotestacea and D. virilis with bacterial and fungal pathogens and quantified AMP expression.
While diptericin in D. virilis was induced by exposure to gram-negative bacteria, it was not induced in D. neotestacea, showing that conservation of immune genes does not necessarily imply conservation of the realized immune response. Our study lends support to the idea that invertebrate AMPs evolve rapidly, and that Drosophila harbor a diverse repertoire of AMPs with potentially important functional consequences.
由于为黑腹果蝇开发了强大的遗传工具，果蝇是研究动物免疫进化的重要模型。然而，果蝇是一个种类极其丰富的谱系，具有广泛的生态、自然历史和多样的天敌。令人惊讶的是，除了黑腹果蝇之外，对其他果蝇物种的免疫系统所做的功能研究非常少。在本研究中，我们研究了果蝇亚属中免疫基因的进化，该亚属大约在2500万至4000万年前从Sophophora亚属（包括黑腹果蝇）分化而来。我们重点研究新黑腹果蝇，这是一种用于研究昆虫与寄生线虫之间相互作用的林地物种，并将最近的转录组数据与感染实验相结合，以阐明宿主免疫的各个方面。
我们发现，参与黑腹果蝇免疫反应的绝大多数基因在新黑腹果蝇中是保守的，但有一些有趣的例外，特别是在抗菌肽（AMPs）方面；直到最近，人们还认为抗菌肽在果蝇中不会快速进化。出乎意料的是，我们在果蝇亚属的果蝇中发现了一种独特的双翅菌素，它似乎是在多样化（正向）选择下进化而来的。我们还描述了抗菌肽果蝇霉素在果蝇亚属中的存在，此前人们认为它仅限于Sophophora亚属。我们用细菌和真菌病原体对果蝇亚属的两个物种，新黑腹果蝇和粗壮果蝇进行了挑战，并对抗菌肽的表达进行了定量。
虽然粗壮果蝇中的双翅菌素在接触革兰氏阴性细菌时会被诱导，但在新黑腹果蝇中却不会，这表明免疫基因的保守性并不一定意味着实际免疫反应的保守性。我们的研究支持了无脊椎动物抗菌肽快速进化的观点，并且果蝇拥有多种抗菌肽，可能具有重要的功能后果。
