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

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 e...

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Main Authors: Cai, Qing, Tulloss, Rodham E, Tang, Li P, Tolgor, Bau, Zhang, Ping, Chen, Zuo H, Yang, Zhu L
Format: Article in Journal/Newspaper
Language:English
Published: BioMed Central Ltd. 2014
Subjects:
Online Access:http://www.biomedcentral.com/1471-2148/14/143
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spelling ftbiomed:oai:biomedcentral.com:1471-2148-14-143 2023-05-15T15:42:42+02:00 Multi-locus phylogeny of lethal amanitas: Implications for species diversity and historical biogeography Cai, Qing Tulloss, Rodham E Tang, Li P Tolgor, Bau Zhang, Ping Chen, Zuo H Yang, Zhu L 2014-06-21 http://www.biomedcentral.com/1471-2148/14/143 en eng BioMed Central Ltd. http://www.biomedcentral.com/1471-2148/14/143 Copyright 2014 Cai et al.; licensee BioMed Central Ltd. Amanita Biogeography Lethal substances Phylogenetic species Molecular clock Synapomorphy Research article 2014 ftbiomed 2014-07-20T00:34:09Z 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. Article in Journal/Newspaper Bering Land Bridge BioMed Central Lagrange ENVELOPE(-62.597,-62.597,-64.529,-64.529)
institution Open Polar
collection BioMed Central
op_collection_id ftbiomed
language English
topic Amanita
Biogeography
Lethal substances
Phylogenetic species
Molecular clock
Synapomorphy
spellingShingle Amanita
Biogeography
Lethal substances
Phylogenetic species
Molecular clock
Synapomorphy
Cai, Qing
Tulloss, Rodham E
Tang, Li P
Tolgor, Bau
Zhang, Ping
Chen, Zuo H
Yang, Zhu L
Multi-locus phylogeny of lethal amanitas: Implications for species diversity and historical biogeography
topic_facet Amanita
Biogeography
Lethal substances
Phylogenetic species
Molecular clock
Synapomorphy
description 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.
format Article in Journal/Newspaper
author Cai, Qing
Tulloss, Rodham E
Tang, Li P
Tolgor, Bau
Zhang, Ping
Chen, Zuo H
Yang, Zhu L
author_facet Cai, Qing
Tulloss, Rodham E
Tang, Li P
Tolgor, Bau
Zhang, Ping
Chen, Zuo H
Yang, Zhu L
author_sort Cai, Qing
title Multi-locus phylogeny of lethal amanitas: Implications for species diversity and historical biogeography
title_short Multi-locus phylogeny of lethal amanitas: Implications for species diversity and historical biogeography
title_full Multi-locus phylogeny of lethal amanitas: Implications for species diversity and historical biogeography
title_fullStr Multi-locus phylogeny of lethal amanitas: Implications for species diversity and historical biogeography
title_full_unstemmed Multi-locus phylogeny of lethal amanitas: Implications for species diversity and historical biogeography
title_sort multi-locus phylogeny of lethal amanitas: implications for species diversity and historical biogeography
publisher BioMed Central Ltd.
publishDate 2014
url http://www.biomedcentral.com/1471-2148/14/143
long_lat ENVELOPE(-62.597,-62.597,-64.529,-64.529)
geographic Lagrange
geographic_facet Lagrange
genre Bering Land Bridge
genre_facet Bering Land Bridge
op_relation http://www.biomedcentral.com/1471-2148/14/143
op_rights Copyright 2014 Cai et al.; licensee BioMed Central Ltd.
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