Phylogeny and historical biogeography of true morels (Morchella) reveals an early Cretaceous origin and high continental endemism and provincialism in the Holarctic

Authors: O Donnell, Kerry; Rooney, Alejandro - Alex; MILLS, GARY - Diversified Natural Products, Inc; KUO, MICHAEL - Eastern Illinois University; WEBER, NANCY - Oregon State University; Rehner, Stephen

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/21/2010
Publication Date: 10/20/2010
Citation: O Donnell, K., Rooney, A.P., Mills, G., Kuo, M., Weber, N.S., Rehner, S.A. 2010. Phylogeny and historical biogeography of true morels (Morchella) reveals an early Cretaceous origin and high continental endemism and provincialism in the Holarctic. Proceedings of the National Academy of Sciences. 48(3):252-265.

Interpretive Summary: Morel mushrooms (Morchella) are arguably the most widely recognized and highly prized of the estimated 1.5 million fungi that inhabit our planet. Although field guides treat these epicurean macrofungi as though the species have worldwide distributions, this assumption has not been tested. Prompted by the results of a growing number of molecular studies, which have shown many macro- and microscopic microbes exhibit strong geographic structure, we investigated their origin, evolutionary diversification and historical biogeography. Diversification time estimates place the origin of Morchella at approximately 129 million years ago within western North America. Morchella appears to have evolved and diversified in the Northern Hemisphere; no species has dispersed into the Southern Hemisphere. The 37 species within North America or Eurasia were found in only one of these two continents. Moreover, 17 of the 19 North American and 16 of the 18 Eurasian species were restricted to either the eastern or western regions of these continents. The only commercially grown species, M. rufobrunnea, was resolved as a novel lineage representing the earliest divergence within the genus. Although morel fruit bodies produce thousands of explosively discharged spores with an ellipsoidal drag-minimizing shape, our results strongly suggest that they are poorly adapted at invading novel niches by long distance dispersal. Furthermore, morel mushrooms appear to have remained remarkably static morphologically for the past 100 million years. Thirty-three of the species were cultured during this study for future biotechnological utilization. Results of the present study represent a significant advance to morel biodiversity and conservation genetics. This research provides mushroom growers, biotechnologists, fungal geneticists and conservation geneticists with a broad spectrum of genetically characterized cultures of morel species which should advance their commercial development, promote studies of the genetics of morel mushroom formation, and provide the basis for formulating sound conservation policies.

Technical Abstract: Morel mushrooms (Morchella, phylum Ascomycota) are arguably the most widely recognized and highly prized of the estimated 1.5 million fungi that inhabit our planet. Although field guides treat these epicurean macrofungi as though the species have cosmopolitan distributions, this assumption has not been tested. Prompted by the results of a growing number of molecular studies, which have shown many macro- and microscopic microbes exhibit strong biogeographic structure, we constructed a 4-gene dataset for 177 members of the Morchellaceae to elucidate their origin, evolutionary diversification and historical biogeography. Diversification time estimates place the origin of the Morchellaceae in the middle Triassic 243.63 million years ago (Mya) and the divergence of Morchella from its closest relatives in the early Cretaceous 129.61 Mya, both within western North America. Phylogenetic analyses identified three lineages within Morchella: a basal monotypic lineage represented by M. rufobrunnea, and two sister clades comprising the black morels (Elata clade, 26 species) and yellow morels (Esculenta clade, 16 species). Morchella possesses a classic Laurasian distribution in that 37 of the 41 species identified were restricted to the Holarctic. Moreover, all 37 Holarctic species exhibited continental endemism and 17 of the 19 North American and 16 of the 18 Eurasian species exhibited provincialism. Although morel fruit bodies produce thousands of explosively discharged spores with an ellipsoidal drag-minimizing shape, our results strongly suggest that they are poorly adapted at invading novel niches. Furthermore, morels also appear to have retained the ancestral fruit body plan, which has remained remarkably static since the Cretaceous.