Abstract

The caterpillar fungus Ophiocordyceps sinensis is one of the most valuable medicinal fungi in the world, and it requires host insects in family Hepialidae (Lepidoptera) to complete its life cycle. However, the genetic diversity and phylogeographic structures of the host insects remain to be explored. We analyzed the genetic diversity and temporal and spatial distribution patterns of genetic variation of the host insects throughout the O. sinensis distribution. Abundant haplotype and nucleotide diversity mainly existed in the areas of Nyingchi, ShangriLa, and around the edge of the Qinghai-Tibet Plateau, where are considered as the diversity center or micro-refuges of the host insects of O. sinensis. However, there was little genetic variation among host insects from 72.1% of all populations, indicating that the host species composition might be relatively simple in large-scale O. sinensis populations. All host insects are monophyletic except for those from four O. sinensis populations around Qinghai Lake. Significant phylogeographic structure (NST>GST, P<0.05) was revealed for the monophyletic host insects, and the three major phylogenetic groups corresponded with specific geographical areas. The divergence of most host insects was estimated to have occurred at ca. 3.7 Ma, shortly before the rapid uplift of the QTP. The geographical distribution and star-like network of the haplotypes implied that most host insects were derived from the relicts of a once-widespread host that subsequently became fragmented. Neutrality tests, mismatch distribution analysis, and expansion time estimation confirmed that most host insects presented recent demographic expansions that began ca. 0.118 Ma in the late Pleistocene. Therefore, the genetic diversity and distribution of the present-day insects should be attributed to effects of the Qinghai-Tibet Plateau uplift and glacial advance/retreat cycles during the Quaternary ice age. These results provide valuable information to guide the protection and sustainable use of these host insects as well as O. sinensis.

Highlights

  • Ophiocordyceps sinensis (Berk.) Sung, Sung, Hywel-Jones and Spatafora (Ascomycota: Ophiocordycipitaceae), a caterpillar fungus [1], has been used for centuries as a traditional Chinese medicine to treat asthma, bronchial/lung infection, and kidney disease [2,3,4]

  • Ophiocordyceps sinensis and its host insects are endemic to the Qinghai-Tibet Plateau (QTP) in western China, i.e., Qinghai, Tibet, Yunnan, Sichuan, and Gansu provinces, where they are mainly distributed in alpine meadows [8,9]

  • Haplotype diversity There were no insertions or deletions of nucleotides in the 654 bp cytochrome oxidase subunit I (COI) sequences amplified from 400 samples from all 43 O. sinensis populations

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Summary

Introduction

Ophiocordyceps sinensis (Berk.) Sung, Sung, Hywel-Jones and Spatafora (Ascomycota: Ophiocordycipitaceae), a caterpillar fungus [1], has been used for centuries as a traditional Chinese medicine to treat asthma, bronchial/lung infection, and kidney disease [2,3,4]. The host insects of O. sinensis belong to the family Hepialidae [5]. The fungus infects their larvae and forms sclerotia within the insect’s intact exoskeleton, enabling the fungus to withstand the winter [6]. Ophiocordyceps sinensis and its host insects are endemic to the Qinghai-Tibet Plateau (QTP) in western China, i.e., Qinghai, Tibet, Yunnan, Sichuan, and Gansu provinces, where they are mainly distributed in alpine meadows [8,9]. This fungus is becoming endangered through both overexploitation because of its commercial value, and habitat degeneration in recent years. There exists an urgent need to establish appropriate strategies/policies to protect the endangered O. sinensis and its host insects

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