title: Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage.
abstract: Truffles have evolved from epigeous (aboveground) ancestors in nearly every major lineage of fleshy fungi. Because accelerated rates of morphological evolution accompany the transition to the truffle form, closely related epigeous ancestors remain unknown for most truffle lineages. This is the case for the quintessential truffle genus Tuber, which includes species with socio-economic importance and esteemed culinary attributes. Ecologically, Tuber spp. form obligate mycorrhizal symbioses with diverse species of plant hosts including pines, oaks, poplars, orchids, and commercially important trees such as hazelnut and pecan. Unfortunately, limited geographic sampling and inconclusive phylogenetic relationships have obscured our understanding of their origin, biogeography, and diversification. To address this problem, we present a global sampling of Tuberaceae based on DNA sequence data from four loci for phylogenetic inference and molecular dating. Our well-resolved Tuberaceae phylogeny shows high levels of regional and continental endemism. We also identify a previously unknown epigeous member of the Tuberaceae--the South American cup-fungus Nothojafnea thaxteri (E.K. Cash) Gamundí. Phylogenetic resolution was further improved through the inclusion of a previously unrecognized Southern hemisphere sister group of the Tuberaceae. This morphologically diverse assemblage of species includes truffle (e.g. Gymnohydnotrya spp.) and non-truffle forms that are endemic to Australia and South America. Southern hemisphere taxa appear to have diverged more recently than the Northern hemisphere lineages. Our analysis of the Tuberaceae suggests that Tuber evolved from an epigeous ancestor. Molecular dating estimates Tuberaceae divergence in the late Jurassic (~156 million years ago), with subsequent radiations in the Cretaceous and Paleogene. Intra-continental diversification, limited long-distance dispersal, and ecological adaptations help to explain patterns of truffle evolution and biodiversity.
authors.affiliation: Deparment of Biology, Duke University, Durham, North Carolina, United States of America. gregory.bonito@duke.edu
authors.forename: Gregory
authors.initials: G
authors.lastname: Bonito
authors.forename: Matthew E
authors.initials: ME
authors.lastname: Smith
authors.forename: Michael
authors.initials: M
authors.lastname: Nowak
authors.forename: Rosanne A
authors.initials: RA
authors.lastname: Healy
authors.forename: Gonzalo
authors.initials: G
authors.lastname: Guevara
authors.forename: Efren
authors.initials: E
authors.lastname: Cázares
authors.forename: Akihiko
authors.initials: A
authors.lastname: Kinoshita
authors.forename: Eduardo R
authors.initials: ER
authors.lastname: Nouhra
authors.forename: Laura S
authors.initials: LS
authors.lastname: Domínguez
authors.forename: Leho
authors.initials: L
authors.lastname: Tedersoo
authors.forename: Claude
authors.initials: C
authors.lastname: Murat
authors.forename: Yun
authors.initials: Y
authors.lastname: Wang
authors.forename: Baldomero Arroyo
authors.initials: BA
authors.lastname: Moreno
authors.forename: Donald H
authors.initials: DH
authors.lastname: Pfister
authors.forename: Kazuhide
authors.initials: K
authors.lastname: Nara
authors.forename: Alessandra
authors.initials: A
authors.lastname: Zambonelli
authors.forename: James M
authors.initials: JM
authors.lastname: Trappe
authors.forename: Rytas
authors.initials: R
authors.lastname: Vilgalys
mesh_terms: D001203:Ascomycota / Q000235:genetics* / Q000502:physiology*; D001499:Bayes Theorem; D005075:Biological Evolution; D002965:Classification; D017931:DNA Primers; D004463:Ecology; D019143:Evolution, Molecular; D005800:Genes, Fungal; D005843:Geography; D016013:Likelihood Functions; D015233:Models, Statistical; D008969:Molecular Sequence Data; D010802:Phylogeny
chemical_list: D017931:DNA Primers