Department of Environmental Sciences, Zoology, University of Basel, Basel 4051, Switzerland.
Genome Biol Evol. 2024 Oct 9;16(10). doi: 10.1093/gbe/evae222.
Genomic regions that play a role in parasite defense are often found to be highly variable, with the major histocompatibility complex serving as an iconic example. Single nucleotide polymorphisms may represent only a small portion of this variability, with Indel polymorphisms and copy number variation further contributing. In extreme cases, haplotypes may no longer be recognized as orthologous. Understanding the evolution of such highly divergent regions is challenging because the most extreme variation is not visible using reference-assisted genomic approaches. Here we analyze the case of the Pasteuria Resistance Complex in the crustacean Daphnia magna, a defense complex in the host against the common and virulent bacterium Pasteuria ramosa. Two haplotypes of this region have been previously described, with parts of it being nonhomologous, and the region has been shown to be under balancing selection. Using pan-genome analysis and tree reconciliation methods to explore the evolution of the Pasteuria Resistance Complex and its characteristics within and between species of Daphnia and other Cladoceran species, our analysis revealed a remarkable diversity in this region even among host species, with many nonhomologous hyper-divergent haplotypes. The Pasteuria Resistance Complex is characterized by extensive duplication and losses of Fucosyltransferase (FuT) and Galactosyltransferase (GalT) genes that are believed to play a role in parasite defense. The Pasteuria Resistance Complex region can be traced back to common ancestors over 250 million years. The unique combination of an ancient resistance complex and a dynamic, hyper-divergent genomic environment presents a fascinating opportunity to investigate the role of such regions in the evolution and long-term maintenance of resistance polymorphisms. Our findings offer valuable insights into the evolutionary forces shaping disease resistance and adaptation, not only in the genus Daphnia, but potentially across the entire Cladocera class.
在寄生虫防御中起作用的基因组区域通常被发现具有高度的可变性，主要组织相容性复合体就是一个典型的例子。单核苷酸多态性可能只代表这种可变性的一小部分，插入缺失多态性和拷贝数变异进一步增加了这种可变性。在极端情况下，单倍型可能不再被视为同源。由于最极端的变异在使用参考辅助基因组方法时不可见，因此理解这种高度分化区域的进化具有挑战性。在这里，我们分析了节肢动物大型溞（Daphnia magna）中的寄生虫抗性复合物（Pasteuria Resistance Complex）的情况，这是宿主针对常见且有毒的细菌巴氏杆菌（Pasteuria ramosa）的防御复合物。该区域的两个单倍型以前曾被描述过，其中部分是非同源的，并且该区域已经显示出处于平衡选择之下。通过泛基因组分析和树协调方法来探索寄生虫抗性复合物及其在 Daphnia 和其他枝角类物种内和物种间的进化和特征，我们的分析揭示了该区域的惊人多样性，即使在宿主物种之间也是如此，存在许多非同源的超分化单倍型。寄生虫抗性复合物的特征是广泛的 FuT 和 GalT 基因的重复和丢失，这些基因被认为在寄生虫防御中起作用。寄生虫抗性复合物区域可以追溯到超过 2.5 亿年前的共同祖先。古老的抗性复合物和动态的、超分化的基因组环境的独特结合，为研究这些区域在抗性多态性的进化和长期维持中的作用提供了一个引人入胜的机会。我们的发现为塑造疾病抗性和适应的进化力量提供了有价值的见解，不仅在大型溞属中，而且可能在整个枝角类目中。
