Open Access Highly Accessed Research article

Multi-locus phylogeny of lethal amanitas: Implications for species diversity and historical biogeography

Qing Cai16, Rodham E Tulloss2, Li P Tang13, Bau Tolgor4, Ping Zhang5, Zuo H Chen5 and Zhu L Yang1*

Author Affiliations

1 Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China

2 Herbarium Rooseveltensis Amanitarum, P. O. Box 57, Roosevelt, New Jersey 08555-0057, USA

3 School of Pharmacology, Kunming Medical University, Kunming, Yunnan 650500, China

4 Institute of Mycology, Jilin Agricultural University, Changchun, Jilin 130118, China

5 College of Life Science, Hunan Normal University, Changsha, Hunan 410081, China

6 University of Chinese Academy of Sciences, Beijing 100039, China

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BMC Evolutionary Biology 2014, 14:143  doi:10.1186/1471-2148-14-143

Published: 21 June 2014

Abstract

Background

Lethal amanitas (Amanita section Phalloideae) are a group of wild, fatal mushrooms causing many poisoning cases worldwide. However, the diversity and evolutionary history of these lethal mushrooms remain poorly known due to the limited sampling and insufficient gene fragments employed for phylogenetic analyses. In this study, five gene loci (nrLSU, ITS, rpb2, ef1-α and β-tubulin) with a widely geographic sampling from East and South Asia, Europe, North and Central America, South Africa and Australia were analysed with maximum-likelihood, maximum-parsimony and Bayesian inference methods. Biochemical analyses were also conducted with intention to detect amatoxins and phalloidin in 14 representative samples.

Result

Lethal amanitas were robustly supported to be a monophyletic group after excluding five species that were provisionally defined as lethal amanitas based on morphological studies. In lethal amanitas, 28 phylogenetic species were recognised by integrating molecular phylogenetic analyses with morphological studies, and 14 of them represented putatively new species. The biochemical analyses indicated a single origin of cyclic peptide toxins (amatoxins and phalloidin) within Amanita and suggested that this kind of toxins seemed to be a synapomorphy of lethal amanitas. Molecular dating through BEAST and biogeographic analyses with LAGRANGE and RASP indicated that lethal amanitas most likely originated in the Palaeotropics with the present crown group dated around 64.92 Mya in the early Paleocene, and the East Asia–eastern North America or Eurasia–North America–Central America disjunct distribution patterns were primarily established during the middle Oligocene to Miocene.

Conclusion

The cryptic diversity found in this study indicates that the species diversity of lethal amanitas is strongly underestimated under the current taxonomy. The intercontinental sister species or sister groups relationships among East Asia and eastern North America or Eurasia–North America–Central America within lethal amanitas are best explained by the diversification model of Palaeotropical origin, dispersal via the Bering Land Bridge, followed by regional vicariance speciation resulting from climate change during the middle Oligocene to the present. These findings indicate the importance of both dispersal and vicariance in shaping the intercontinental distributions of these ectomycorrhizal fungi.

Keywords:
Amanita; Biogeography; Lethal substances; Phylogenetic species; Molecular clock; Synapomorphy