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

historic drought over evolutionary time in western North America gradually shaped tectoni- cally-derived drainage systems, resulting in the erosion of genetic diversity, with populations of endemic fish repeatedly collapsing into refugia then expanding outward during more pluvial periods [64]. Episodic flooding, on the other hand, allowed antecedent streams to down-cut, with headwaters subsequently eroding, basins concomitantly expanding, with large-scale dispers- als being promoted [65]. Such alterations (i.e., captures, diversions, beheadings; [66]) not only extended fishes into adjacent basins [67] but also facilitated hybridization [68–70], a process that has (and continues to) confound both taxonomic resolution and management strategies. Flows within basins are often abridged by longitudinal barriers that are vicariant for larger-bodied species, yet serve as passive filters for fishes smaller and more limited in dis- persal capacity [71]. As a result, fish distributions represent a series of biogeographic ’islands’ within and among basins, each reflecting local expansions, contractions, and extinctions. This process provides a necessary template from which to gauge the response of fishes to similar tectonic, orogenic, and climatic impacts within dendritic riverscapes less well moni- tored (as herein). The Himalaya provides such a template as shaped by tectonic and climatic events. Its sharp elevational gradients derived via orogeny provided ample opportunities for diversification. For

example, many deeply incised valleys emerged along the border of the elevating QTP, and given their increasing gradients, subsequently transitioned into prominent geomorphic fea- tures. As a result, many unique physiographic characteristics emerged, particularly when com- pared with other large global river networks. For example, five (of 10) QTP rivers [i.e., Yellow, upper Yangtze (= Jinsha), upper Mekong (= Lancang), upper Salween (= Nujiang), and Yar- lung-Tsangpo (= upper Brahmaputra)] originate at >4,500m elevation, flow >1,000km to the border of the QTP, and subsequently drop >3,000m to Asian lowlands. Interestingly, the Mekong, Salween, and Yangtze flow in parallel for ~170km, and achieve their closest proximity at <70km (Fig 1B; [72]). In S1 Appendix, we provide references that link divergence intervals for our phylogeographic clades with geomorphic/ climatic drivers in the Himalaya. These events, in turn, have established the region as a global hotspot for biodiversity ende- mism [21, 73] with Snowtrout as a characteristic element of the aquatic fauna. A more specific example is found within the YLTR, where a deep canyon derived via orogeny effectively parti- tioned S. oconnori [74], promoting several distinct ESUs (Evolutionarily Significant Units; [75]). This vicariance similarly impacted S. waltoni (BA tree; [76]), but those components are evolutionarily less distinct and designated instead as MUs (Management Units; [75]). Studies of Himalayan freshwater most often focused on select regions, rivers, and/or moun-

tains [77–80]. Our approach broadens that perspective, in that we fill biogeographic gaps in the Himalaya and leverage existing data to more fully evaluate origin and subsequent dispersal of Snowtrout across Asia. Table 2. Statistical topology tests comparing maximum likelihood (ML) and Bayesian (BA) phylogenetic results (= Tree). logL = Log Likelihood value; deltaL = logL difference from maximal logL in the set; Bp-RELL = Bootstrap proportions using RELL method (weights sum to 1 across trees); p-KH = p-value of one-sided Kishino- Hasegawa test; p-SH = p-value of Shimodaira-Hasegawa test; c-ELW = Expected Likelihood Weight (weights sum to 1 across trees); p-AU = p-value of Approximately Unbiased test. A plus sign (+) next to a p-value denotes 95% confidence sets, whereas a minus sign (-) denotes a significant exclusion (i.e., the tree is rejected). All tests stemmed from 1,000 resamples using the RELL method. Tree logL deltaL bp-RELL p-KH p-SH c-ELW p-AU ML -9526.83 0.0 0.986 + 0.986 + 1.00 + 0.978 + 0.985 + BA -9582.76 55.93 0.014 - 0.013 - 0.013 - 0.014 - 0.015 - https://doi.org/10.1371/journal.pone.0289736.t002 PLOS ONE Himalayan uplift and aquatic evolution PLOS ONE | https://doi.org/10.1371/journal.pone.0289736 October 24, 2023 15 / 27