1 Introduction

Mountains exhibit extraordinarily heterogeneous environments and host a remarkable diversity of (endemic) terrestrial and aquatic species (Rahbek et al., 2019; Rahbek et al., 2019; Perrigo et al., 2020). Since Alexander von Humboldt initiated the principle of Cosmos (“unity of nature”) that combines geology and biology to explain the distribution patterns of life (Von Humboldt, 1860), researchers have attempted to explore how geophysical modifications over time, such as orogeny and climate change, could have influenced biological processes involved in speciation and diversification (Ding et al., 2020). To better understand the origin and evolution of biodiversity in mountains, we investigate four caddisfly species living in the highest and largest mountain system in the world: the Tibeto-Himalayan Region.
The Himalayas and the adjacent Hengduan Mountains (HM) have drawn increasing interest from biogeographers and ecologists (Favre et al., 2015; Hoorn et al., 2018; Muellner-Riehl, 2019; Rahbek et al., 2019), especially after Myers et al. (2000) classified these mountain systems as two of the global biodiversity hotspots. In recent years, biogeographic studies on the Tibeto-Himalayan Region have revealed that the evolution of species was profoundly shaped by changes in geomorphology and climate over millions of years (e.g., Favre et al., 2015; Xing & Ree, 2017; Mosbrugger et al., 2018; Muellner‐Riehl et al., 2019; Rana et al., 2019; Ding et al., 2020; Rana et al., 2022). For instance, Ding et al. (2020) revealed that in situ speciation, diversification, and colonization in the alpine flora inhabiting the HM, the Himalayas, and the Qinghai-Tibetan Plateau were jointly driven by mountain uplift and intensification of the Asian monsoon system. Nonetheless, different topographic relief, orogenic activity, and climate history in the Himalayas and the HM led to distinct biodiversity patterns (Ding et al., 2020). For example, species richness increases from west to east in birds (Price et al., 2011), plants (Yan et al., 2013; Bhattarai et al., 2014; Rana et al., 2019), and mammals (Srinivasan et al., 2014). This parallels the increase of precipitation towards the east in the Himalayas. In contrast, a North-South floristic divide was revealed in the HM, which may be associated with both climate (separation by the line of regular freezing) and topography (divided by the Jinsha River, Li et al., 2021). Moreover, patterns of biodiversity in the HM appear to have been more dynamic through time: diversity hotspots of montane plants have shifted from the southeastern to the central and western parts of the HM between the last glacial maximum (LGM) to today (Liang et al., 2018). The phylogeographic history of the HM is further complicated by the presence of geographically extensive and long-lasting barriers to dispersal such as the deeply incised valleys of the Irrawaddy, the Salween, the Mekong and the Yangtze rivers, which have been shown to be instrumental in delineating floristic motifs in the region (Li et al., 2021; Muellner‐Riehl & Favre, 2021). Therefore, biogeographers and ecologists have increasingly viewed evolutionary processes in these two mountain systems as relatively independent despite their biogeographical interconnection (e.g., Ding et al., 2020).
The “mountain-geobiodiversity hypothesis (MGH)” conceptualizes the link between geophysical changes and the origin and evolution of biodiversity based on the Tibeto-Himalayan Region (Mosbrugger et al. 2018). In this hypothesis three boundary conditions are deemed essential to the accumulation of biodiversity in mountains: (i) full elevational zonation with lowland, montane, and alpine zones; (ii) the occurrence of a species-pump driven by climatic fluctuation; and (iii) strong environmental gradients. Within this conceptual framework, mountain uplift provides elevational gradients and locally diverse topography. This condition increases opportunities for local or regional taxa to adapt to a high variety of niches (i), and fosters a higher resistance to climate change via vertical displacement (iii). Meanwhile, during climate fluctuations, for instance in the Quaternary, diversification is fostered by a species-pump effect (ii) via cyclical range fragmentation (causing divergence) and secondary contacts (involving hybridization or reinforcement) (Mosbrugger et al., 2018; Muellner-Riehl, 2019). This hypothesis was partially verified on a few taxa from the HM (e.g., Fu et al., 2020, 2022; Wang et al., 2022), while some global-scale meta-analyses also support it (Muellner‐Riehl et al., 2019). However, case studies have so far been limited to plant taxa, such that the validation and refining of the hypothesis for a broader taxonomic spectrum is missing. Following Favre et al. (2015), which provided a generalized overview of the origin and evolution of mountain biodiversity, we investigate the MGH in the context of the diversification of species of the aquatic insect genusHimalopsyche (Trichoptera, Rhyacophilidae).
Himalopsyche is a genus of aquatic caddisflies that inhabit mountains. Most Himalopsyche species are distributed in Central and East Asia (Hjalmarsson et al., 2019) except for the NearcticH. phryganea (Ross, 1941). Like all caddisflies, species ofHimalopsyche have a merolimnic life cycle and are considered important bioindicators (Resh & Unzicker, 1975; Tsuruishi et al., 2006; Hjalmarsson, 2019; Morse et al. 2019). The larvae of this taxon generally inhabit turbulent, fast-flowing rivers and streams where they live as ferocious predators (Hjalmarsson et al., 2018). Currently, there are 56 described species in the genus (Hjalmarsson et al., 2019), with 23 occurring in the Himalayas and 34 occurring in the HM (some of them distributed in both). The center of diversity of the genusHimalopsyche is located in these two mountain regions. But regionally, different species exhibit strongly differentiated niches usually associated with elevational gradients (Schmid & Botosaneanu, 1966). For example, some species inhabit lower elevations between 1500–2500 m.a.s.l., as in the case of H. digitata (Martynov, 1935, in the Himalayas) or H. platon (Malicky, 2011, in the HM), whereas other species prefer higher elevation ranges between 2000–4500 m.a.s.l., such as H. tibetana (Martynov, 1930, in the Himalayas) and H. gregoryi (Ulmer, 1932, in the HM; summarized in Hjalmarsson 2020). As reported by Lehrian et al. (2009), montane caddisflies that inhabit different elevation ranges but have similar geographic distributions may exhibit distinct population structures putatively associated with varying dispersal capabilities, habitat specificity or differences in phylogeographic history. Because species of Himalopsyche inhabit different elevations, they are a good model for investigating how geography has shaped their genetic diversity over time.
For aquatic species, distribution patterns and dispersal among habitats are constrained by the dendritic structure of the stream network (Tonkin et al., 2018). To assess and interpret differing patterns of population structure in aquatic insects, Finn et al. (2007) and Hughes et al. (2013) proposed process-based models of population genetic diversity patterns that account for the structure of drainage systems: the stream hierarchy model, the death valley model, the headwater model, isolation by distance and panmixia (or also called as the widespread gene flow model, Hughes, 2007). These models are assigned to a given species primarily by their population connectivity, defined by the level of gene flow among populations throughout the drainage networks. The population connectivity generally depends on (1) traits that determine dispersal ability (dispersal ability and behaviour, life cycle, oviposition, and the spatial distribution of source populations) (Smith & Smith, 2009; Parkyn & Smith, 2011); (2) the distance between populations; (3) the suitability of the new habitat; and (4) the permeability of the landscape (Rader et al., 2019). In caddisflies, dispersal is often an “along-stream” movement as defined in the context of the “colonization cycle” (Müller, 1954; Collier & Smith, 1997; Petersen et al., 2004; Winterbourn et al., 2007). Current-induced downstream movements often occur in the larval stage. Part of this downstream movement is then compensated by adult females (and also males) flying upstream prior to mating or egg-laying. However, adults also fly perpendicular to the stream (lateral dispersal) and thus disperse overland between catchments allowing gene flow between caddisfly populations from different catchments (Svensson, 1974; Malicky, 1987; Collier & Smith, 1997; Griffith et al., 1998; Bowler & Benton, 2005; Wilcock et al., 2007; Smith & Smith, 2009; Engelhardt et al., 2011; Müller-Peddinghaus, 2011; Deng et al., 2021b). A genomic study on a species complex of the Himalopsyche revealed that continuous gene flow can be maintained over millions of years between two basins (Deng et al., 2021b). Hence, in addition to elevational zonation (i) and environmental gradients (iii) as proposed in the MGH, and because of the unique dispersal ability of caddisflies, drainage systems may also be crucial topographical features that drive distribution ranges of caddisflies, e.g. through the species-pump effect (ii).
To examine these patterns across both the Himalayas and HM, we studied four Himalopsyche species from the two mountains. For each mountain range, we chose a species that inhabits high elevation streams,H. tibetana (Himalayas) and H. gregoryi (HM), and another species that inhabits lower elevations, H. digitata (Himalayas) and H. platon (HM). We combined population genomics analysis of 333 individuals across the four species with species distribution model (SDM) to (1) reveal the genetic pattern of species inhabiting high-elevation versus low-elevation, and species from the Himalayas versus the HM, (2) evaluate the role of environmental factors including climate change, mountain topography and drainage rearrangement on the evolution of aquatic biodiversity in the Tibeto-Himalayan Region, and (3) assess the implication of the MGH in different mountain systems such as the Himalayas and the HM.