Cheng Shao-Chen, Liu Chun-Bing, Yao Xue-Qin, Hu Jing-Yang, Yin Ting-Ting, Lim Burton K, Chen Wu, Wang Guo-Dong, Zhang Cheng-Lin, Irwin David M, Zhang Zhi-Gang, Zhang Ya-Ping, Yu Li
State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, School of Life Sciences, Yunnan University, Kunming 650091, China.
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
Natl Sci Rev. 2022 Aug 24;10(4):nwac174. doi: 10.1093/nsr/nwac174. eCollection 2023 Apr.
Highly specialized myrmecophagy (ant- and termite-eating) has independently evolved multiple times in species of various mammalian orders and represents a textbook example of phenotypic evolutionary convergence. We explored the mechanisms involved in this unique dietary adaptation and convergence through multi-omic analyses, including analyses of host genomes and transcriptomes, as well as gut metagenomes, in combination with validating assays of key enzymes' activities, in the species of three mammalian orders (anteaters, echidnas and pangolins of the orders Xenarthra, Monotremata and Pholidota, respectively) and their relatives. We demonstrate the complex and diverse interactions between hosts and their symbiotic microbiota that have provided adaptive solutions for nutritional and detoxification challenges associated with high levels of protein and lipid metabolisms, trehalose degradation, and toxic substance detoxification. Interestingly, we also reveal their spatially complementary cooperation involved in degradation of ants' and termites' chitin exoskeletons. This study contributes new insights into the dietary evolution of mammals and the mechanisms involved in the coordination of physiological functions by animal hosts and their gut commensals.
高度特化的食蚁性(以蚂蚁和白蚁为食)在各种哺乳动物目物种中多次独立进化,是表型进化趋同的典型例子。我们通过多组学分析,包括对宿主基因组和转录组以及肠道宏基因组的分析,并结合关键酶活性的验证试验,在三个哺乳动物目(分别为异关节目、单孔目和鳞甲目的食蚁兽、针鼹和穿山甲)及其亲属物种中,探索了这种独特饮食适应和趋同所涉及的机制。我们证明了宿主与其共生微生物群之间复杂多样的相互作用,这些相互作用为与高水平蛋白质和脂质代谢、海藻糖降解以及有毒物质解毒相关的营养和解毒挑战提供了适应性解决方案。有趣的是,我们还揭示了它们在降解蚂蚁和白蚁几丁质外骨骼方面的空间互补合作。这项研究为哺乳动物的饮食进化以及动物宿主及其肠道共生体协调生理功能所涉及的机制提供了新的见解。