Abstract

Simple SummaryHimalopsyche is a group of aquatic insects endemic to the Hengduan Mountains, of which species are usually easily identifiable based on male genitalia, except for a few morphologically variable groups including the Himalopsyche martynovi complex. In order to clarify species boundaries within this complex, we investigated its evolutionary history (phylogenetics and gene flow analyses) using a large genomic dataset (~500,000 sites). We found three clades in the Himalopsyche martynovi complex, one of which being very variable morphologically while being involved in gene flow with other related lineages. When interpreted in the light of past geological, climatic and palaeohydrological changes, our study suggests that biological novelty—here, trait variation and recombination—may have been acquired via hybridization and represent a source of mountain biodiversity.The Hengduan Mountains are one of the most species-rich mountainous areas in the world. The origin and evolution of such a remarkable biodiversity are likely to be associated with geological or climatic dynamics, as well as taxon-specific biotic processes (e.g., hybridization, polyploidization, etc.). Here, we investigate the mechanisms fostering the diversification of the endemic Himalopsyche martynovi complex, a poorly known group of aquatic insects. We used multiple allelic datasets generated from 691 AHE loci to reconstruct species and RaxML phylogenetic trees. We selected the most reliable phylogenetic tree to perform network and gene flow analyses. The phylogenetic reconstructions and network analysis identified three clades, including H. epikur, H. martynovi sensu stricto and H. cf. martynovi. Himalopsyche martynovi sensu stricto and H. cf. martynovi present an intermediate morphology between H. epikur and H. viteceki, the closest known relative to the H. martynovi-complex. The gene flow analysis revealed extensive gene flow among these lineages. Our results suggest that H. viteceki and H. epikur are likely to have contributed to the evolution of H. martynovi sensu stricto and H. cf. martynovi via gene flow, and thus, our study provides insights in the diversification process of a lesser-known ecological group, and hints at the potential role of gene flow in the emergence of biological novelty in the Hengduan Mountains.

Highlights

  • The distribution of species diversity is globally uneven [1,2,3], and areas with an exceptional concentration of species are often qualified as ‘biodiversity hotspots’ depending on their current degradation and need for conservation [4,5]

  • “mountain-geobiodiversity hypothesis” [11], patterns of increased diversification in mountain areas are associated with three boundary conditions, including a full elevational zonation (i), a high ruggedness of the terrain providing environmental gradients (ii), as well as climate oscillations which facilitate mountain systems to act as “species-pumps”, i.e., they serve as the background for repeated pulses of elevational migration leading to fragmentation and speciation followed by species expansions over large time scales [11] (iii)

  • We found that species of the H. martynovi-complex, and H. martynovi s.s., cannot be distinguished morphologically because of the high versatility of trait morphology in the male genitalia, whereas our phylogeny unequivocally recovers three robust lineages in this species complex

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Summary

Introduction

The distribution of species diversity is globally uneven [1,2,3], and areas with an exceptional concentration of species are often qualified as ‘biodiversity hotspots’ depending on their current degradation and need for conservation [4,5]. As suggested in the “mountain-geobiodiversity hypothesis” [11], patterns of increased diversification in mountain areas (and in the region of the QTP) are associated with three boundary conditions, including a full elevational zonation (i), a high ruggedness of the terrain providing environmental gradients (ii), as well as climate oscillations which facilitate mountain systems to act as “species-pumps”, i.e., they serve as the background for repeated pulses of elevational migration leading to fragmentation and speciation followed by species expansions over large time scales [11] (iii). Strongly overlap temporally with climate oscillations (iii) of the last few million years, at least in plants [10] During these more recent times, cyclical climatic modifications may have fostered alternate phases of species’ range fragmentation (allopatric differentiation) and secondary contact, upon which gene flow among species or populations with incomplete reproductive isolation may have occurred. Species complexes are common in the Hengduan Mts (e.g., plant [14], mammal [15], fungus [16], caddisflies [17]) and represent good models for studying evolutionary processes and mechanisms of speciation in the context of the mountain-geobiodiversity hypothesis

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