Phylogenomics, biogeography, and trait evolution of the Boletaceae (Boletales, Agaricomycetes, Basidiomycota)

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Abstract

The species-rich porcini mushroom family Boletaceae is a widespread and well-known group of ectomycorrhizal (ECM) mushroom-forming fungi that has eluded intrafamilial phylogenetic resolution despite many attempts using morphological traits and multi-locus molecular datasets. In this study, we present a genome-wide molecular dataset 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 an early diverging lineage within the 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 cladogenesis patterns that parallel its fragmentation. Ancestral state reconstruction of sporocarp morphological traits predicts that the ancestor of the Boletaceae was lamellate with ornamented basidiospores, contrary to most contemporary “bolete” morphologies. Transition rates indicated that the lamellate hymenophore and sequestrate sporocarp are reversible traits. Together, this study represents the most comprehensively sampled, data-rich molecular phylogeny of the Boletaceae to date, enabling robust inferences of trait evolution and biogeography in the group.

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  1. rates

    It's very relevant whether a species tree vs "specimen tree" was used here, as the inclusion of specimen here could change interpretation of rates quite significantly

  2. +j

    Okay, yes, so I'd check to see whether the parameter estimates under a model without the jump parameter are consistent with these results, or if the J model has led to very different biological conclusions.

  3. Biogeographic reconstruction using BioGeoBEARS.

    I'll reiterate again (and hopefully I'm mistaken!) that if this tree includes both distinct species and multiple specimens from the same species, application of ancestral range (or state) reconstruction is not correct. These methods should only be applied to a species or a uniform taxonomic rank/biological unit

  4. A summary coalescent species tree was constructed from the resulting gene trees using hybrid-ASTRAL implemented in ASTER (v1.15) (Zhang and Mirarab 2022).

    Am I correct in understanding that in this hybrid-ASTRAL tree, you have collapsed specimen into distinct species? If so, how many species in total?

    If not, this poses problems for the ancestral state and ancestral range reconstruction, as each should only be applied to a single taxonomic rank (i.e. species), rather than multiple (i.e. species and individuals sampled from different populations)

  5. b) lineages-through-time plot calculated with the “ltt.plot” function in the R pack-age “ape.”

    This is not reported in the methods section, but should be.

    Additionally, if I'm understanding correctly, is each tip in this tree a specimen, not a distinct species? If so, it does not make sense to use a lineage through time plot here unless you have retained only a single representative per species.

  6. most likely model

    Related to my other comment, if the best-fit model was one that included the "jump" parameter "+J", this would be consistent with a demonstrated pathological favoring of such models, independent of whether such a model is biologically sensible.

    See Ree and Sanmartín 2018 for more: https://doi.org/10.1111/jbi.13173

  7. The most likely model was chosen according to AIC and weighted AIC score calculated in BioGeoBEARS.

    Which models did you fit? These details - both the models you fitted, and their relative fits to the data - really must be reported here in the methods. Unless I'm missing something, they don't seem to be reported in the supplement either.