Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi

Pradeep K. Divakar; Ana Crespo; Mats Wedin; Steven D. Leavitt; David L. Hawksworth; Leena Myllys; Bruce Mccune; Tiina Randlane; Jarle W. Bjerke; Yoshihito Ohmura; Imke Schmitt; Carlos G. Boluda; David Alors; Beatriz Roca-Valiente; Ruth Del-Prado; Constantino Ruibal; Kawinnat Buaruang; Jano Núñez-Zapata; Guillermo Amo de Paz; Víctor J. Rico; M. Carmen Molina; John A. Elix; Theodore L. Esslinger; Inger Kristin K. Tronstad; Hanna Lindgren; Damien Ertz; Cécile Gueidan; Lauri Saag; Kristiina Mark; Garima Singh; Francesco Dal Grande; Sittiporn Parnmen; Andreas Beck; Michel Navarro Benatti; Dan Blanchon; Mehmet Candan; Philippe Clerc; Trevor Goward; Martin Grube; Brendan P. Hodkinson; Jae Seoun Hur; Gintaras Kantvilas; Paul M. Kirika; James Lendemer; Jan Eric Mattsson; María Inés Messuti; Jolanta Miadlikowska; Matthew Nelsen; Jan I. Ohlson; Sergio Pérez-Ortega; Andres Saag; Harrie J.M. Sipman; Mohammad Sohrabi; Arne Thell; Göran Thor; Camille Truong; Rebecca Yahr; Dalip K. Upreti; Paloma Cubas; H. Thorsten Lumbsch

doi:10.1111/nph.13553

Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi

Pradeep K. Divakar^*, Ana Crespo, Mats Wedin, Steven D. Leavitt, David L. Hawksworth, Leena Myllys, Bruce Mccune, Tiina Randlane, Jarle W. Bjerke, Yoshihito Ohmura, Imke Schmitt, Carlos G. Boluda, David Alors, Beatriz Roca-Valiente, Ruth Del-Prado, Constantino Ruibal, Kawinnat Buaruang, Jano Núñez-Zapata, Guillermo Amo de Paz, Víctor J. RicoM. Carmen Molina, John A. Elix, Theodore L. Esslinger, Inger Kristin K. Tronstad, Hanna Lindgren, Damien Ertz, Cécile Gueidan, Lauri Saag, Kristiina Mark, Garima Singh, Francesco Dal Grande, Sittiporn Parnmen, Andreas Beck, Michel Navarro Benatti, Dan Blanchon, Mehmet Candan, Philippe Clerc, Trevor Goward, Martin Grube, Brendan P. Hodkinson, Jae Seoun Hur, Gintaras Kantvilas, Paul M. Kirika, James Lendemer, Jan Eric Mattsson, María Inés Messuti, Jolanta Miadlikowska, Matthew Nelsen, Jan I. Ohlson, Sergio Pérez-Ortega, Andres Saag, Harrie J.M. Sipman, Mohammad Sohrabi, Arne Thell, Göran Thor, Camille Truong, Rebecca Yahr, Dalip K. Upreti, Paloma Cubas, H. Thorsten Lumbsch

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

102 Citations (Scopus)

Abstract

We studied the evolutionary history of the Parmeliaceae (Lecanoromycetes, Ascomycota), one of the largest families of lichen-forming fungi with complex and variable morphologies, also including several lichenicolous fungi. We assembled a six-locus data set including nuclear, mitochondrial and low-copy protein-coding genes from 293 operational taxonomic units (OTUs). The lichenicolous lifestyle originated independently three times in lichenized ancestors within Parmeliaceae, and a new generic name is introduced for one of these fungi. In all cases, the independent origins occurred c. 24 million yr ago. Further, we show that the Paleocene, Eocene and Oligocene were key periods when diversification of major lineages within Parmeliaceae occurred, with subsequent radiations occurring primarily during the Oligocene and Miocene. Our phylogenetic hypothesis supports the independent origin of lichenicolous fungi associated with climatic shifts at the Oligocene-Miocene boundary. Moreover, diversification bursts at different times may be crucial factors driving the diversification of Parmeliaceae. Additionally, our study provides novel insight into evolutionary relationships in this large and diverse family of lichen-forming ascomycetes.

Original language	English
Pages (from-to)	1217-1226
Number of pages	10
Journal	New Phytologist
Volume	208
Issue number	4
DOIs	https://doi.org/10.1111/nph.13553
Publication status	Published - Dec 2015

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Divakar, P. K., Crespo, A., Wedin, M., Leavitt, S. D., Hawksworth, D. L., Myllys, L., Mccune, B., Randlane, T., Bjerke, J. W., Ohmura, Y., Schmitt, I., Boluda, C. G., Alors, D., Roca-Valiente, B., Del-Prado, R., Ruibal, C., Buaruang, K., Núñez-Zapata, J., Amo de Paz, G., ... Lumbsch, H. T. (2015). Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi. New Phytologist, 208(4), 1217-1226. https://doi.org/10.1111/nph.13553

@article{d439531cae3848dea66e3c04c43b765d,

title = "Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi",

abstract = "We studied the evolutionary history of the Parmeliaceae (Lecanoromycetes, Ascomycota), one of the largest families of lichen-forming fungi with complex and variable morphologies, also including several lichenicolous fungi. We assembled a six-locus data set including nuclear, mitochondrial and low-copy protein-coding genes from 293 operational taxonomic units (OTUs). The lichenicolous lifestyle originated independently three times in lichenized ancestors within Parmeliaceae, and a new generic name is introduced for one of these fungi. In all cases, the independent origins occurred c. 24 million yr ago. Further, we show that the Paleocene, Eocene and Oligocene were key periods when diversification of major lineages within Parmeliaceae occurred, with subsequent radiations occurring primarily during the Oligocene and Miocene. Our phylogenetic hypothesis supports the independent origin of lichenicolous fungi associated with climatic shifts at the Oligocene-Miocene boundary. Moreover, diversification bursts at different times may be crucial factors driving the diversification of Parmeliaceae. Additionally, our study provides novel insight into evolutionary relationships in this large and diverse family of lichen-forming ascomycetes.",

keywords = "Ancestral character reconstruction, Ascomycota, Lichenicolous fungi, Mutualism, Parmeliaceae, Phylogeny, Raesaenenia",

author = "Divakar, {Pradeep K.} and Ana Crespo and Mats Wedin and Leavitt, {Steven D.} and Hawksworth, {David L.} and Leena Myllys and Bruce Mccune and Tiina Randlane and Bjerke, {Jarle W.} and Yoshihito Ohmura and Imke Schmitt and Boluda, {Carlos G.} and David Alors and Beatriz Roca-Valiente and Ruth Del-Prado and Constantino Ruibal and Kawinnat Buaruang and Jano N{\'u}{\~n}ez-Zapata and {Amo de Paz}, Guillermo and Rico, {V{\'i}ctor J.} and Molina, {M. Carmen} and Elix, {John A.} and Esslinger, {Theodore L.} and Tronstad, {Inger Kristin K.} and Hanna Lindgren and Damien Ertz and C{\'e}cile Gueidan and Lauri Saag and Kristiina Mark and Garima Singh and {Dal Grande}, Francesco and Sittiporn Parnmen and Andreas Beck and Benatti, {Michel Navarro} and Dan Blanchon and Mehmet Candan and Philippe Clerc and Trevor Goward and Martin Grube and Hodkinson, {Brendan P.} and Hur, {Jae Seoun} and Gintaras Kantvilas and Kirika, {Paul M.} and James Lendemer and Mattsson, {Jan Eric} and Messuti, {Mar{\'i}a In{\'e}s} and Jolanta Miadlikowska and Matthew Nelsen and Ohlson, {Jan I.} and Sergio P{\'e}rez-Ortega and Andres Saag and Sipman, {Harrie J.M.} and Mohammad Sohrabi and Arne Thell and G{\"o}ran Thor and Camille Truong and Rebecca Yahr and Upreti, {Dalip K.} and Paloma Cubas and Lumbsch, {H. Thorsten}",

note = "Publisher Copyright: {\textcopyright} 2015 New Phytologist Trust.",

year = "2015",

month = dec,

doi = "10.1111/nph.13553",

language = "English",

volume = "208",

pages = "1217--1226",

journal = "New Phytologist",

issn = "0028-646X",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "4",

}

Divakar, PK, Crespo, A, Wedin, M, Leavitt, SD, Hawksworth, DL, Myllys, L, Mccune, B, Randlane, T, Bjerke, JW, Ohmura, Y, Schmitt, I, Boluda, CG, Alors, D, Roca-Valiente, B, Del-Prado, R, Ruibal, C, Buaruang, K, Núñez-Zapata, J, Amo de Paz, G, Rico, VJ, Molina, MC, Elix, JA, Esslinger, TL, Tronstad, IKK, Lindgren, H, Ertz, D, Gueidan, C, Saag, L, Mark, K, Singh, G, Dal Grande, F, Parnmen, S, Beck, A, Benatti, MN, Blanchon, D, Candan, M, Clerc, P, Goward, T, Grube, M, Hodkinson, BP, Hur, JS, Kantvilas, G, Kirika, PM, Lendemer, J, Mattsson, JE, Messuti, MI, Miadlikowska, J, Nelsen, M, Ohlson, JI, Pérez-Ortega, S, Saag, A, Sipman, HJM, Sohrabi, M, Thell, A, Thor, G, Truong, C, Yahr, R, Upreti, DK, Cubas, P & Lumbsch, HT 2015, 'Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi', New Phytologist, vol. 208, no. 4, pp. 1217-1226. https://doi.org/10.1111/nph.13553

TY - JOUR

T1 - Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi

AU - Divakar, Pradeep K.

AU - Crespo, Ana

AU - Wedin, Mats

AU - Leavitt, Steven D.

AU - Hawksworth, David L.

AU - Myllys, Leena

AU - Mccune, Bruce

AU - Randlane, Tiina

AU - Bjerke, Jarle W.

AU - Ohmura, Yoshihito

AU - Schmitt, Imke

AU - Boluda, Carlos G.

AU - Alors, David

AU - Roca-Valiente, Beatriz

AU - Del-Prado, Ruth

AU - Ruibal, Constantino

AU - Buaruang, Kawinnat

AU - Núñez-Zapata, Jano

AU - Amo de Paz, Guillermo

AU - Rico, Víctor J.

AU - Molina, M. Carmen

AU - Elix, John A.

AU - Esslinger, Theodore L.

AU - Tronstad, Inger Kristin K.

AU - Lindgren, Hanna

AU - Ertz, Damien

AU - Gueidan, Cécile

AU - Saag, Lauri

AU - Mark, Kristiina

AU - Singh, Garima

AU - Dal Grande, Francesco

AU - Parnmen, Sittiporn

AU - Beck, Andreas

AU - Benatti, Michel Navarro

AU - Blanchon, Dan

AU - Candan, Mehmet

AU - Clerc, Philippe

AU - Goward, Trevor

AU - Grube, Martin

AU - Hodkinson, Brendan P.

AU - Hur, Jae Seoun

AU - Kantvilas, Gintaras

AU - Kirika, Paul M.

AU - Lendemer, James

AU - Mattsson, Jan Eric

AU - Messuti, María Inés

AU - Miadlikowska, Jolanta

AU - Nelsen, Matthew

AU - Ohlson, Jan I.

AU - Pérez-Ortega, Sergio

AU - Saag, Andres

AU - Sipman, Harrie J.M.

AU - Sohrabi, Mohammad

AU - Thell, Arne

AU - Thor, Göran

AU - Truong, Camille

AU - Yahr, Rebecca

AU - Upreti, Dalip K.

AU - Cubas, Paloma

AU - Lumbsch, H. Thorsten

PY - 2015/12

Y1 - 2015/12

N2 - We studied the evolutionary history of the Parmeliaceae (Lecanoromycetes, Ascomycota), one of the largest families of lichen-forming fungi with complex and variable morphologies, also including several lichenicolous fungi. We assembled a six-locus data set including nuclear, mitochondrial and low-copy protein-coding genes from 293 operational taxonomic units (OTUs). The lichenicolous lifestyle originated independently three times in lichenized ancestors within Parmeliaceae, and a new generic name is introduced for one of these fungi. In all cases, the independent origins occurred c. 24 million yr ago. Further, we show that the Paleocene, Eocene and Oligocene were key periods when diversification of major lineages within Parmeliaceae occurred, with subsequent radiations occurring primarily during the Oligocene and Miocene. Our phylogenetic hypothesis supports the independent origin of lichenicolous fungi associated with climatic shifts at the Oligocene-Miocene boundary. Moreover, diversification bursts at different times may be crucial factors driving the diversification of Parmeliaceae. Additionally, our study provides novel insight into evolutionary relationships in this large and diverse family of lichen-forming ascomycetes.

AB - We studied the evolutionary history of the Parmeliaceae (Lecanoromycetes, Ascomycota), one of the largest families of lichen-forming fungi with complex and variable morphologies, also including several lichenicolous fungi. We assembled a six-locus data set including nuclear, mitochondrial and low-copy protein-coding genes from 293 operational taxonomic units (OTUs). The lichenicolous lifestyle originated independently three times in lichenized ancestors within Parmeliaceae, and a new generic name is introduced for one of these fungi. In all cases, the independent origins occurred c. 24 million yr ago. Further, we show that the Paleocene, Eocene and Oligocene were key periods when diversification of major lineages within Parmeliaceae occurred, with subsequent radiations occurring primarily during the Oligocene and Miocene. Our phylogenetic hypothesis supports the independent origin of lichenicolous fungi associated with climatic shifts at the Oligocene-Miocene boundary. Moreover, diversification bursts at different times may be crucial factors driving the diversification of Parmeliaceae. Additionally, our study provides novel insight into evolutionary relationships in this large and diverse family of lichen-forming ascomycetes.

KW - Ancestral character reconstruction

KW - Ascomycota

KW - Lichenicolous fungi

KW - Mutualism

KW - Parmeliaceae

KW - Phylogeny

KW - Raesaenenia

UR - http://www.scopus.com/inward/record.url?scp=84946498212&partnerID=8YFLogxK

U2 - 10.1111/nph.13553

DO - 10.1111/nph.13553

M3 - Article

SN - 0028-646X

VL - 208

SP - 1217

EP - 1226

JO - New Phytologist

JF - New Phytologist

IS - 4

ER -

Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi

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