Global Evolutionary and Transmission Dynamics of Transmissible Gastroenteritis Virus, 1952–2023

doi:10.1016/j.jia.2025.09.026

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Wenqiang Wang^1*, Qilin Zhao^1*, Zhenbang Zhu¹, Wei Wen¹, Xiangdong Li^{1, 2#}

¹Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou 225009, China

²Joint International Research Laboratory of Agriculture and Agri-Product Safety, the Ministry of Education of China, Yangzhou University, Yangzhou 225009, China

Highlights

TGEV comprises three genotypes with distinct geographic distribution patterns.

Adaptive evolution of TGEV is shaped by recombination and the host–virus arms race.

China serves as the major hub for global transmission of TGEV.

Abstract
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摘要

猪传染性胃肠炎病毒（Transmissible gastroenteritis virus, TGEV）是一种猪源肠道冠状病毒，长期以来对全球养猪业构成了严重威胁。然而，TGEV的生态学特征、进化历史及其跨区域传播格局仍缺乏系统认识。本研究旨在揭示TGEV的进化动力学与全球传播模式，从而为病毒的防控提供科学依据。

本研究收集了1952—2023年全球67条TGEV完整基因组，并通过系统发育分析、比较基因组学、重组检测、选择压力分析、单倍型网络构建及贝叶斯地理扩散模型，对TGEV的进化过程和传播路径进行了系统的研究。

研究结果显示，TGEV可划分为三种主要基因型：其一是具有洲际分布并呈现混合特征的GIa基因型；其二是主要分布于欧洲的GIb基因型；其三是仅限于美国的GII基因型。重组分析发现，GIa基因型的ORF1a与S基因区存在多次重组事件，这些基因变化可能推动了TGEV的进化。选择压力分析表明，S基因处于强烈的正选择作用之下，其中五个位点受到显著选择压力，提示宿主-病毒间的“进化军备竞赛”可能加速了TGEV的适应与多样化。单倍型网络分析发现，美国来源的毒株具有最高的遗传多样性，而中国毒株则以两个核心单倍型为主，并伴随多个紧密相关的小单倍型。贝叶斯地理扩散分析结果证实，中国在TGEV的全球传播中发挥了关键作用，并揭示了其传播至美国、越南等地的具体路径。

综上所述，本研究首次基于全球时间跨度超过70年的全基因组数据系统阐明了TGEV的进化历史和全球传播格局，揭示了重组与宿主-病毒相互作用在其适应性进化中的重要作用。研究结果不仅加深了对TGEV生态学和进化机制的理解，也为未来制定更具针对性的防控策略提供了理论参考。

Abstract

Transmissible gastroenteritis virus (TGEV) is an enteric coronavirus that poses a significant threat to the swine industry. However, the ecology, evolutionary history, and transmission dynamics of TGEV remain poorly understood. In this study, we analyzed 67 complete TGEV genomes collected globally between 1952 and 2023, employing comparative genomics to uncover the evolutionary dynamics and spatial dissemination of TGEV. Our findings reveal that TGEV can be classified into three major genotypes: the admixed GIa lineage with intercontinental distribution, the Europe-specific GIb lineage, and the U.S.-restricted GII lineage. Recombination events were identified in the ORF1a and S gene regions of GIa strains, suggesting that these genetic changes may have contributed to the evolutionary diversification of TGEV. Notably, the S gene is under strong positive selection, with five key codons under selection pressure, suggesting that the potential host–virus evolutionary arms race accelerates TGEV adaptation and diversification. Haplotype network analysis revealed that U.S. strains exhibit the highest genetic diversity, while Chinese strains are characterized by two dominant haplotypes surrounded by multiple closely related minor haplotypes. Bayesian phylogeographic analysis further confirmed that China has played an important role in the global dissemination of TGEV and clarified its transmission routes to regions such as the United States and Vietnam. Overall, this study advances our understanding of the evolution and spread of TGEV, and may contribute to the development of more effective strategies for its prevention and control.

Keywords: TGEV evolution recombination selection phylogeography epidemiology

Online: 23 September 2025

Fund:

This work was supported by the National Key Research and Development Program of China (2023YFD1800500), the Jiangsu Innovative and Entrepreneurial Talent Team Project, China (JSSCTD202224), the 111 Project D18007, the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD) and the High Performance Computing Cluster of College of Veterinary Medicine, Yangzhou University, China.

About author: Wenqiang Wang, E-mail: wqwang@yzu.edu.cn; Qilin Zhao, E-mail: 2224236752@qq.com #Correspondence Xiangdong Li, Tel: +86-15298450032, E-mail: 007352@yzu.edu.cn * These authors contributed equally to this study.

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Wenqiang Wang, Qilin Zhao, Zhenbang Zhu, Wei Wen, Xiangdong Li. 2025. Global Evolutionary and Transmission Dynamics of Transmissible Gastroenteritis Virus, 1952–2023. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.09.026

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