Publications by authors named "Rodham E Tulloss"

10 Publications

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Megaphylogeny resolves global patterns of mushroom evolution.

Nat Ecol Evol 2019 04 18;3(4):668-678. Epub 2019 Mar 18.

Synthetic and Systems Biology Unit, Biological Research Centre, Hungarian Academy of Sciences, Szeged, Hungary.

Mushroom-forming fungi (Agaricomycetes) have the greatest morphological diversity and complexity of any group of fungi. They have radiated into most niches and fulfil diverse roles in the ecosystem, including wood decomposers, pathogens or mycorrhizal mutualists. Despite the importance of mushroom-forming fungi, large-scale patterns of their evolutionary history are poorly known, in part due to the lack of a comprehensive and dated molecular phylogeny. Here, using multigene and genome-based data, we assemble a 5,284-species phylogenetic tree and infer ages and broad patterns of speciation/extinction and morphological innovation in mushroom-forming fungi. Agaricomycetes started a rapid class-wide radiation in the Jurassic, coinciding with the spread of (sub)tropical coniferous forests and a warming climate. A possible mass extinction, several clade-specific adaptive radiations and morphological diversification of fruiting bodies followed during the Cretaceous and the Paleogene, convergently giving rise to the classic toadstool morphology, with a cap, stalk and gills (pileate-stipitate morphology). This morphology is associated with increased rates of lineage diversification, suggesting it represents a key innovation in the evolution of mushroom-forming fungi. The increase in mushroom diversity started during the Mesozoic-Cenozoic radiation event, an era of humid climate when terrestrial communities dominated by gymnosperms and reptiles were also expanding.
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http://dx.doi.org/10.1038/s41559-019-0834-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6443077PMC
April 2019

Considerations and consequences of allowing DNA sequence data as types of fungal taxa.

Authors:
Juan Carlos Zamora Måns Svensson Roland Kirschner Ibai Olariaga Svengunnar Ryman Luis Alberto Parra József Geml Anna Rosling Slavomír Adamčík Teuvo Ahti M Catherine Aime A Martyn Ainsworth László Albert Edgardo Albertó Alberto Altés García Dmitry Ageev Reinhard Agerer Begoña Aguirre-Hudson Joe Ammirati Harry Andersson Claudio Angelini Vladimír Antonín Takayuki Aoki André Aptroot Didier Argaud Blanca Imelda Arguello Sosa Arne Aronsen Ulf Arup Bita Asgari Boris Assyov Violeta Atienza Ditte Bandini João Luís Baptista-Ferreira Hans-Otto Baral Tim Baroni Robert Weingart Barreto Henry Beker Ann Bell Jean-Michel Bellanger Francesco Bellù Martin Bemmann Mika Bendiksby Egil Bendiksen Katriina Bendiksen Lajos Benedek Anna Bérešová-Guttová Franz Berger Reinhard Berndt Annarosa Bernicchia Alona Yu Biketova Enrico Bizio Curtis Bjork Teun Boekhout David Boertmann Tanja Böhning Florent Boittin Carlos G Boluda Menno W Boomsluiter Jan Borovička Tor Erik Brandrud Uwe Braun Irwin Brodo Tatiana Bulyonkova Harold H Burdsall Bart Buyck Ana Rosa Burgaz Vicent Calatayud Philippe Callac Emanuele Campo Massimo Candusso Brigitte Capoen Joaquim Carbó Matteo Carbone Rafael F Castañeda-Ruiz Michael A Castellano Jie Chen Philippe Clerc Giovanni Consiglio Gilles Corriol Régis Courtecuisse Ana Crespo Cathy Cripps Pedro W Crous Gladstone Alves da Silva Meiriele da Silva Marjo Dam Nico Dam Frank Dämmrich Kanad Das Linda Davies Eske De Crop Andre De Kesel Ruben De Lange Bárbara De Madrignac Bonzi Thomas Edison E Dela Cruz Lynn Delgat Vincent Demoulin Dennis E Desjardin Paul Diederich Bálint Dima Maria Martha Dios Pradeep Kumar Divakar Clovis Douanla-Meli Brian Douglas Elisandro Ricardo Drechsler-Santos Paul S Dyer Ursula Eberhardt Damien Ertz Fernando Esteve-Raventós Javier Angel Etayo Salazar Vera Evenson Guillaume Eyssartier Edit Farkas Alain Favre Anna G Fedosova Mario Filippa Péter Finy Adam Flakus Simón Fos Jacques Fournier André Fraiture Paolo Franchi Ana Esperanza Franco Molano Gernot Friebes Andreas Frisch Alan Fryday Giuliana Furci Ricardo Galán Márquez Matteo Garbelotto Joaquina María García-Martín Mónica A García Otálora Dania García Sánchez Alain Gardiennet Sigisfredo Garnica Isaac Garrido Benavent Genevieve Gates Alice da Cruz Lima Gerlach Masoomeh Ghobad-Nejhad Tatiana B Gibertoni Tine Grebenc Irmgard Greilhuber Bella Grishkan Johannes Z Groenewald Martin Grube Gérald Gruhn Cécile Gueidan Gro Gulden Luis Fp Gusmão Josef Hafellner Michel Hairaud Marek Halama Nils Hallenberg Roy E Halling Karen Hansen Christoffer Bugge Harder Jacob Heilmann-Clausen Stip Helleman Alain Henriot Margarita Hernandez-Restrepo Raphaël Herve Caroline Hobart Mascha Hoffmeister Klaus Høiland Jan Holec Håkon Holien Karen Hughes Vit Hubka Seppo Huhtinen Boris Ivančević Marian Jagers Walter Jaklitsch AnnaElise Jansen Ruvishika S Jayawardena Thomas Stjernegaard Jeppesen Mikael Jeppson Peter Johnston Per Magnus Jørgensen Ingvar Kärnefelt Liudmila B Kalinina Gintaras Kantvilas Mitko Karadelev Taiga Kasuya Ivona Kautmanová Richard W Kerrigan Martin Kirchmair Anna Kiyashko Dániel G Knapp Henning Knudsen Kerry Knudsen Tommy Knutsson Miroslav Kolařík Urmas Kõljalg Alica Košuthová Attila Koszka Heikki Kotiranta Vera Kotkova Ondřej Koukol Jiří Kout Gábor M Kovács Martin Kříž Åsa Kruys Viktor Kučera Linas Kudzma Francisco Kuhar Martin Kukwa T K Arun Kumar Vladimír Kunca Ivana Kušan Thomas W Kuyper Carlos Lado Thomas Læssøe Patrice Lainé Ewald Langer Ellen Larsson Karl-Henrik Larsson Gary Laursen Christian Lechat Serena Lee James C Lendemer Laura Levin Uwe Lindemann Håkan Lindström Xingzhong Liu Regulo Carlos Llarena Hernandez Esteve Llop Csaba Locsmándi Deborah Jean Lodge Michael Loizides László Lőkös Jennifer Luangsa-Ard Matthias Lüderitz Thorsten Lumbsch Matthias Lutz Dan Mahoney Ekaterina Malysheva Vera Malysheva Patinjareveettil Manimohan Yasmina Marin-Felix Guilhermina Marques Rubén Martínez-Gil Guy Marson Gerardo Mata P Brandon Matheny Geir Harald Mathiassen Neven Matočec Helmut Mayrhofer Mehdi Mehrabi Ireneia Melo Armin Mešić Andrew S Methven Otto Miettinen Ana M Millanes Romero Andrew N Miller James K Mitchell Roland Moberg Pierre-Arthur Moreau Gabriel Moreno Olga Morozova Asunción Morte Lucia Muggia Guillermo Muñoz González Leena Myllys István Nagy László G Nagy Maria Alice Neves Tuomo Niemelä Pier Luigi Nimis Nicolas Niveiro Machiel E Noordeloos Anders Nordin Sara Raouia Noumeur Yuri Novozhilov Jorinde Nuytinck Esteri Ohenoja Patricia Oliveira Fiuza Alan Orange Alexander Ordynets Beatriz Ortiz-Santana Leticia Pacheco Ferenc Pál-Fám Melissa Palacio Zdeněk Palice Viktor Papp Kadri Pärtel Julia Pawlowska Aurelia Paz Ursula Peintner Shaun Pennycook Olinto Liparini Pereira Pablo Pérez Daniëls Miquel À Pérez-De-Gregorio Capella Carlos Manuel Pérez Del Amo Sergio Pérez Gorjón Sergio Pérez-Ortega Israel Pérez-Vargas Brian A Perry Jens H Petersen Ronald H Petersen Donald H Pfister Chayanard Phukhamsakda Marcin Piątek Meike Piepenbring Raquel Pino-Bodas Juan Pablo Pinzón Esquivel Paul Pirot Eugene S Popov Orlando Popoff María Prieto Álvaro Christian Printzen Nadezhda Psurtseva Witoon Purahong Luis Quijada Gerhard Rambold Natalia A Ramírez Huzefa Raja Olivier Raspé Tania Raymundo Martina Réblová Yury A Rebriev Juan de Dios Reyes García Miguel Ángel Ribes Ripoll Franck Richard Mike J Richardson Víctor J Rico Gerardo Lucio Robledo Flavia Rodrigues Barbosa Cristina Rodriguez-Caycedo Pamela Rodriguez-Flakus Anna Ronikier Luis Rubio Casas Katerina Rusevska Günter Saar Irja Saar Isabel Salcedo Sergio M Salcedo Martínez Carlos A Salvador Montoya Santiago Sánchez-Ramírez J Vladimir Sandoval-Sierra Sergi Santamaria Josiane Santana Monteiro Hans Josef Schroers Barbara Schulz Geert Schmidt-Stohn Trond Schumacher Beatrice Senn-Irlet Hana Ševčíková Oleg Shchepin Takashi Shirouzu Anton Shiryaev Klaus Siepe Esteban B Sir Mohammad Sohrabi Karl Soop Viacheslav Spirin Toby Spribille Marc Stadler Joost Stalpers Soili Stenroos Ave Suija Stellan Sunhede Sten Svantesson Sigvard Svensson Tatyana Yu Svetasheva Krzysztof Świerkosz Heidi Tamm Hatira Taskin Adrien Taudière Jan-Olof Tedebrand Raúl Tena Lahoz Marina Temina Arne Thell Marco Thines Göran Thor Holger Thüs Leif Tibell Sanja Tibell Einar Timdal Zdenko Tkalčec Tor Tønsberg Gérard Trichies Dagmar Triebel Andrei Tsurykau Rodham E Tulloss Veera Tuovinen Miguel Ulloa Sosa Carlos Urcelay François Valade Ricardo Valenzuela Garza Pieter van den Boom Nicolas Van Vooren Aida M Vasco-Palacios Jukka Vauras Juan Manuel Velasco Santos Else Vellinga Annemieke Verbeken Per Vetlesen Alfredo Vizzini Hermann Voglmayr Sergey Volobuev Wolfgang von Brackel Elena Voronina Grit Walther Roy Watling Evi Weber Mats Wedin Øyvind Weholt Martin Westberg Eugene Yurchenko Petr Zehnálek Huang Zhang Mikhail P Zhurbenko Stefan Ekman

IMA Fungus 2018 Jun 24;9(1):167-175. Epub 2018 May 24.

Museum of Evolution, Uppsala University, Norbyvägen 16, 75236 Uppsala, Sweden.

Nomenclatural type definitions are one of the most important concepts in biological nomenclature. Being physical objects that can be re-studied by other researchers, types permanently link taxonomy (an artificial agreement to classify biological diversity) with nomenclature (an artificial agreement to name biological diversity). Two proposals to amend the International Code of Nomenclature for algae, fungi, and plants (ICN), allowing DNA sequences alone (of any region and extent) to serve as types of taxon names for voucherless fungi (mainly putative taxa from environmental DNA sequences), have been submitted to be voted on at the 11 International Mycological Congress (Puerto Rico, July 2018). We consider various genetic processes affecting the distribution of alleles among taxa and find that alleles may not consistently and uniquely represent the species within which they are contained. Should the proposals be accepted, the meaning of nomenclatural types would change in a fundamental way from physical objects as sources of data to the data themselves. Such changes are conducive to irreproducible science, the potential typification on artefactual data, and massive creation of names with low information content, ultimately causing nomenclatural instability and unnecessary work for future researchers that would stall future explorations of fungal diversity. We conclude that the acceptance of DNA sequences alone as types of names of taxa, under the terms used in the current proposals, is unnecessary and would not solve the problem of naming putative taxa known only from DNA sequences in a scientifically defensible way. As an alternative, we highlight the use of formulas for naming putative taxa (candidate taxa) that do not require any modification of the ICN.
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http://dx.doi.org/10.5598/imafungus.2018.09.01.10DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6048565PMC
June 2018

In and out of refugia: historical patterns of diversity and demography in the North American Caesar's mushroom species complex.

Mol Ecol 2015 12 20;24(23):5938-56. Epub 2015 Nov 20.

Department of Natural History, Royal Ontario Museum, 100 Queen's Park, Toronto, ON, M5S 2C6, Canada.

Some of the effects of past climate dynamics on plant and animal diversity make-up have been relatively well studied, but to less extent in fungi. Pleistocene refugia are thought to harbour high biological diversity (i.e. phylogenetic lineages and genetic diversity), mainly as a product of increased reproductive isolation and allele conservation. In addition, high extinction rates and genetic erosion are expected in previously glaciated regions. Some of the consequences of past climate dynamics might involve changes in range and population size that can result in divergence and incipient or cryptic speciation. Many of these dynamic processes and patterns can be inferred through phylogenetic and coalescent methods. In this study, we first delimit species within a group of closely related edible ectomycorrhizal Amanita from North America (the American Caesar's mushrooms species complex) using multilocus coalescent-based approaches; and then address questions related to effects of Pleistocene climate change on the diversity and genetics of the group. Our study includes extensive geographical sampling throughout the distribution range, and DNA sequences from three nuclear protein-coding genes. Results reveal cryptic diversity and high speciation rates in refugia. Population sizes and expansions seem to be larger at midrange latitudes (Mexican highlands and SE USA). Range shifts are proportional to population size expansions, which were overall more common during the Pleistocene. This study documents responses to past climate change in fungi and also highlights the applicability of the multispecies coalescent in comparative phylogeographical analyses and diversity assessments that include ancestral species.
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http://dx.doi.org/10.1111/mec.13413DOI Listing
December 2015

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

BMC Evol Biol 2014 06 21;14:143. Epub 2014 Jun 21.

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

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.
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http://dx.doi.org/10.1186/1471-2148-14-143DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4094918PMC
June 2014

Evolutionary consequences of putative intra-and interspecific hybridization in agaric fungi.

Mycologia 2013 Nov-Dec;105(6):1577-94. Epub 2013 Aug 8.

Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee 37996-1100.

Agaric fungi of the southern Appalachian Mountains including Great Smoky Mountains National Park are often heterozygous for the rDNA internal transcribed spacer region (ITS) with >42% of collections showing some heterozygosity for indels and/or base-pair substitutions. For these collections, intra-individual haplotype divergence is typically less than 2%, but for 3% of these collections intra-individual haplotype divergence exceeds that figure. We hypothesize that high intra-individual haplotype divergence is due to hybridization between agaric fungi with divergent haplotypes, possibly migrants from geographically isolated glacial refugia. Four species with relatively high haplotype divergence were examined: Armillaria mellea, Amanita citrina f. lavendula, Gymnopus dichrous and the Hygrocybe flavescens/chlorophana complex. The ITS region was sequenced, haplotypes of heterozygotes were resolved through cloning, and phylogenetic analyses were used to determine the outcome of hybridization events. Within Armillaria mellea and Amanita citrina f. lavendula, we found evidence of interbreeding and recombination. Within G. dichrous and H. flavescens/chlorophana, hybrids were identified but there was no evidence for F2 or higher progeny in natural populations suggesting that the hybrid fruitbodies might be an evolutionary dead end and that the genetically divergent Mendelian populations from which they were derived are, in fact, different species. The association between ITS haplotype divergence of less than 5% (Armillaria mellea = 2.6% excluding gaps; Amanita citrina f. lavendula = 3.3%) with the presence of putative recombinants and greater than 5% (Gymnopus dichrous = 5.7%; Hygrocybe flavescens/chlorophana = 14.1%) with apparent failure of F1 hybrids to produce F2 or higher progeny in populations may suggest a correlation between genetic distance and reproductive isolation.
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http://dx.doi.org/10.3852/13-041DOI Listing
January 2014

The irreversible loss of a decomposition pathway marks the single origin of an ectomycorrhizal symbiosis.

PLoS One 2012 18;7(7):e39597. Epub 2012 Jul 18.

FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts, United States of America.

Microbial symbioses have evolved repeatedly across the tree of life, but the genetic changes underlying transitions to symbiosis are largely unknown, especially for eukaryotic microbial symbionts. We used the genus Amanita, an iconic group of mushroom-forming fungi engaged in ectomycorrhizal symbioses with plants, to identify both the origins and potential genetic changes maintaining the stability of this mutualism. A multi-gene phylogeny reveals one origin of the symbiosis within Amanita, with a single transition from saprotrophic decomposition of dead organic matter to biotrophic dependence on host plants for carbon. Associated with this transition are the losses of two cellulase genes, each of which plays a critical role in extracellular decomposition of organic matter. However a third gene, which acts at later stages in cellulose decomposition, is retained by many, but not all, ectomycorrhizal species. Experiments confirm that symbiotic Amanita species have lost the ability to grow on complex organic matter and have therefore lost the capacity to live in forest soils without carbon supplied by a host plant. Irreversible losses of decomposition pathways are likely to play key roles in the evolutionary stability of these ubiquitous mutualisms.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0039597PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3399872PMC
March 2013

Lateral gene transfer occurring in haloarchaea: an interpretative imitation study.

World J Microbiol Biotechnol 2012 Sep 4;28(9):2913-8. Epub 2012 Jul 4.

Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China.

Lateral gene transfer (LGT) plays an important role in the molecular evolution of haloarchaea. Polyethylene glycol-mediated LGT in haloarchaea has been demonstrated in the laboratory, yet few explanations have been put forward for the apparently common, natural occurrence of plentiful plasmids within haloarchaeal cells. In this study, LGT was induced in two genera of haloarchaea, Haloferax and Halorubrum, by modification of salt concentration of media-a factor that may vary naturally in native haloarchaeal habitat. Minimal growth salt concentrations (MGSCs) of four strains of haloarchaea from these two genera were established, and transformations using two circular double-stranded DNAs (dsDNAs), pSY1 and pWL102, were then produced in media at strain-appropriate MGSCs. The four strains of haloarchaea were transformed successfully by both kinds of dsDNAs with an efficiency of 10(2)-10(3) transformants per microgram dsDNA. The transformation under reduced salt concentration may be an imitation of natural LGT of dsDNA into haloarchaea when salinity in normally hypersaline environments is altered by sudden introduction of fresh water--for example, by rainfall, snow-melt, or flooding--providing a reasonable interpretation for haloarchaea being naturally richer in plasmids than any other known organisms.
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http://dx.doi.org/10.1007/s11274-012-1101-7DOI Listing
September 2012

Amanita lippiae: a new species from the semi-arid caatinga region of Brazil.

Mycologia 2009 Nov-Dec;101(6):864-70

Universidade Federal de Pernambuco, Departamento de Micologia/CCB, Avenida Prof. Nelson Chaves, s/n, CEP: 50670-901, Recife, PE, Brazil.

Amanita lippiae is described as a new species from a semi-arid (caatinga) region of northeastern Brazil. It possesses clampless basidia and elongate to nearly cylindrical inamyloid basidiospores, bears irregular remains of universal veil on the stipe bulb and is a gemmatoid species assignable to Amanita sect. Amanita.
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http://dx.doi.org/10.3852/08-106DOI Listing
December 2009

Evidence for strong inter- and intracontinental phylogeographic structure in Amanita muscaria, a wind-dispersed ectomycorrhizal basidiomycete.

Mol Phylogenet Evol 2008 Aug 29;48(2):694-701. Epub 2008 Apr 29.

Institute of Arctic Biology, University of Alaska Fairbanks, 311 Irving I Building, 902 N. Koyukuk Drive, P.O. Box 757000, Fairbanks, AK 99775-7000, USA.

A growing number of molecular studies show that many fungi have phylogeographic structures and that their distinct lineages are usually limited to different continents. As a conservative test of the extent to which wind-dispersed mycorrhizal fungi may exhibit phylogeographic structure, we chose to study Amanita muscaria, a host-generalist, widespread, wind-dispersed fungus. In this paper, we document the existence of several distinct phylogenetic species within A. muscaria, based on multilocus DNA sequence data. According to our findings, A. muscaria has strong intercontinental genetic disjunctions, and, more surprisingly, has strong intracontinental phylogeographic structure, particularly within North America, often corresponding to certain habitats and/or biogeographic provinces. Our results indicate that the view of A. muscaria as a common, widespread, easily identifiable, ecologically plastic fungus with a wide niche does not correctly represent the ecological and biological realities. On the contrary, the strong associations between phylogenetic species and different habitats support the developing picture of ecoregional endemisms and relatively narrow to very narrow niches for some lineages.
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http://dx.doi.org/10.1016/j.ympev.2008.04.029DOI Listing
August 2008