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.