A revised phylogeny of Boletaceae using whole genome sequences

ABSTRACT

The porcini mushroom family Boletaceae is a diverse, widespread group of ectomycorrhizal (ECM) mushroom-forming fungi that so far has eluded intrafamilial phylogenetic resolution based on morphology and multilocus data sets. In this study, we present a genome-wide molecular data set of 1764 single-copy gene families from a global sampling of 418 Boletaceae specimens. The resulting phylogenetic analysis has strong statistical support for most branches of the tree, including the first statistically robust backbone. The enigmatic Phylloboletellus chloephorus from non-ECM Argentinian subtropical forests was recovered as a new subfamily sister to the core Boletaceae. Time-calibrated branch lengths estimate that the family first arose in the early to mid-Cretaceous and underwent a rapid radiation in the Eocene, possibly when the ECM nutritional mode arose with the emergence and diversification of ECM angiosperms. Biogeographic reconstructions reveal a complex history of vicariance and episodic long-distance dispersal correlated with historical geologic events, including Gondwanan origins and inferred vicariance associated with its disarticulation. Together, this study represents the most comprehensively sampled, data-rich molecular phylogeny of the Boletaceae to date, establishing a foundation for future robust inferences of biogeography in the group.

KEYWORDS:

• Boletales
• evolutionary radiation
• gondwana
• phylogenomics
• porcini

AKNOWLEDGMENTS

We are grateful for field assistance in Madagascar by the staff at the Kew Madagascar Conservation Centre, especially Franck Rakotonasolo, in Cameroon by Dr. Olivier Séne, the National Herbarium of Cameroon and the European Union’s Central African Forestry Ecosystems program at the Dja Faunal Reserve, and in Sarawak by Dr. Sepiah Muid and Dr. Mohamad Hasnul Bolhassan, Universiti Malaysia Sarawak, and the staff at Gunung Mulu National Park and Batang Ai National Park. B.D. is grateful for the support of the Study Visit program at the Singapore Botanic Gardens and multiple grants from the Bentham-Moxon Trust at the Royal Botanic Gardens, Kew. Numerous people made field work possible to which we are very grateful for their help and expertise. We would like to thank Dr. Roy Halling for specimens, discussions, and contributions to the manuscript, and Dr. Sven Buerki for specimens. Anonymous reviewers provided valuable comments on earlier drafts of the manuscript.

DISCLOSURE STATEMENT

No potential conflict of interest was reported by the author(s).

DATA AVAILABILITY STATEMENT

All whole genome sequences are deposited on the National Center for Bioinformation Technology (NCBI) Short Read Archive under the bioproject accession ID Bioproject PRJNA1022813. Genome assemblies are also deposited on the dryad data repository (https://doi.org/10.5061/dryad.dv41ns25n). BUSCO gene alignments, individual gene trees, and our summary coalescent species tree are publicly available on figshare (https://figshare.com/projects/Tremble_et_al_2023_BoletaceaePhylogeny/184027).

SUPPLEMENTARY MATERIAL

Supplemental data for this article can be accessed online at https://doi.org/10.1080/00275514.2024.2314963

Additional information

Funding

This work was supported by the National Science Foundation Directorate for Biological Sciences (NSF-DEB) awards DEB-2114785 to B.D., DEB-0918591 to T.H., DEB-1556338 to T.H. and B.D., and National Geographic Society’s Committee for Research and Exploration grants 6679-99, 7435-03, and 8481-08 to T.H. J.-M.M. was supported by grants from the Royal Ontario Museum (ROM) Governors and the Natural Sciences and Engineering Research Council of Canada, Discovery Program.