The Himalayan uplift and evolution of aquatic biodiversity across Asia: Snowtrout (Cyprininae: Schizothorax) as a test case

biodiversity must be defined and conserved through broad, trans-national collaborations. Our study provides an initial baseline for this process. Introduction The Himalaya is the most extensive and recently evolved mountain system on Earth (length = 2,400km; width = 240km; elevation = 75–8,800m), with global significance under- scored by large-scale lithospheric, cryospheric, and atmospheric interactions [1]. These have not only driven global climate, but also defined the cultural and biological endemism of the region [2]. The Himalaya is topographically separated into three components: Western Hima- laya: ~880 km wide region framed by Indus and Kali Gandaki rivers (southwestern Tibet Autonomous Region of China to western Nepal, respectively); Central Himalaya: ~800 km wide area contained between the Kali Gandaki and Tista rivers (from western Nepal to Sikkim, India, respectively) and; Eastern Himalaya: ~720 km stretch delimited by the Tista and Brah- maputra rivers (from Sikkim to Arunachal Pradesh in India) (https://www.pmfias.com/ himalayas-regional-divisions-punjab-himalayas-assam-himalayas-western-himalayas-central- himalayas-eastern-himalayas/). Massive, tectonically derived mountain chains such as the Himalaya are fundamental in establishing global biodiversity gradients, but strong signals of vicariance and local adaptation are generally noted within terrestrial rather than aquatic sys- tems [3]. Here we evaluate how orogeny (the deformation and folding of Earth’s crust by lat-

eral compression) has contributed to the potential diversification of freshwater fishes broadly across Asia by quantifying phylogeographic and phylogenetic patterns withing a an endemic high-elevation fish genus (Schizothorax). We use these data to infer a potential evolutionary hypothesis for the genus, and offer the resulting perspective as a surrogate for other aquatic biodiversity components in the region. Orogeny and biodiversity of the study region The Himalaya formed as a series of parallel ranges bordered by rivers to the west (Indus) and east (Brahmaputra). It encompasses most of northern Pakistan, northern India (Kashmir to the west, Assam to the east), as well as Nepal, Bhutan, and parts of China, with the extensive Qinghai-Tibetan Plateau (QTP) to the north and the alluvial plains of India and Bangladesh to the south (Fig 1A). It evolved over a 30 Ma span, as one component of the extensive impact between the Indian craton and the Eurasian landmass [4]. This uplift established the Himalaya as a topographic entity and profoundly influenced the connectivity of its regional rivers [5, 6]. In late Oligocene–early Miocene (26–19 Ma), the Yar- lung-Tsangpo River (= YLTR; average elevation 4,000m) formed on the southern border of the QTP as an east-west series of lakes with south-flowing tributaries (Fig 11 in [7]). These lakes eventually coalesced into a westward flowing river (early–mid Miocene; 19–15 Ma) that even- tually reversed its flow in response to a continuing plateau uplift. The YLTR was captured on

the eastern QTP by the Brahmaputra River in early-mid Miocene (i.e., ~18–15 Ma) [6, 8]. The uplift of the QTP was a signature event that seemingly allowed aquatic biodiversity to disperse broadly from west to east, with subsequent access to south-flowing Himalayan drainages even- tually truncated by continued uplift [9]. Three stratigraphic zones subsequently emerged, as manifested by the contemporary spe- cies richness of terrestrial biodiversity [4]. Although this endemism has been hypothesized as driven by tectonic activity, requisite data are either sporadic or absent [10]. Freshwater fish divergence seemingly occurred concomitantly, with tributaries increasingly isolated as the PLOS ONE Himalayan uplift and aquatic evolution PLOS ONE | https://doi.org/10.1371/journal.pone.0289736 October 24, 2023 2 / 27 OR373093 58puza006 OR373094 58tink001 OR373095 58karo003 OR373096. Funding: Author(s) received no specific funding for this work. Competing interests: Authors have declared that no competing interests exist.