New species and emendations of Orphella: taxonomic and phylogenetic reassessment of the genus to establish the Orphellales, for stonefly gut fungi with a twist

ABSTRACT

We consolidate and present data for the sexual stages of five North American species of Orphella, fungal members of trichomycetes previously classified within Harpellales. Three species emendations accommodate the newly recognized characters, including not only the coiled zygospores and accompanying cells but also other morphological traits not provided in the original descriptions for O. avalonensis, O. haysii, and O. hiemalis. We describe three new species, Orphella cataloochensis from both the Smoky Mountains in USA and two provinces in Canada as well as O. pseudoavalonensis and O. pseudohiemalis, both from the Cascade Range, in Oregon, USA. Key morphological features for all known species are summarized and reviewed, with illustrations of some of the North American taxa to update and supplement the literature. The entire suite of morphological characters is discussed, with emphasis on species relationships and hypotheses on possible vicariant origins. We also present a molecular phylogeny based on nuc rDNA 18S and 28S, which supports Orphella as a lineage distinct from Harpellales, and we establish a new order, Orphellales, for it. With the combination of sexual features, now known for 12 of the 14 species of Orphella, and new molecular data, the group is now better characterized, facilitating and hopefully also promoting future studies toward a better understanding of their relationships, origins, and evolutionary history as stonefly gut–dwelling fungi.

KEYWORDS:

• Kickxellomycotina
• Plecoptera
• symbiosis
• Trichomycetes
• Zoopagomycota
• Zygomycota
• 4 new taxa

ACKNOWLEDGMENTS

Prior surveys and collections included colleagues and students. Notably, Marvin C. Williams took part in the Colorado surveys and helped work up slides on O. haysii and Stephen Peterson and Marty Huss for O. hiemalis in Oklahoma. Murray Colbo was our guide and colleague in Newfoundland while we were collecting there, and Charles (Eddie) Beard joined us for part of the survey in the Smoky Mountains. Asako M. Yamamura offered IDs, as we began dissecting, that quickly guided our pursuit and chase of the new species from Oregon, while based at the H.J. Andrews Station. Boris Kondratieff has consistently helped with stonefly IDs for M.M.W. as well as Don Huggins, and Paul Liechti with earlier collections for R.W.L. Other facilities have been used for earlier surveys and have been listed in prior papers, but the University of Tennessee, Department of Botany field station, Harkness Laboratory of Fisheries Research, Algonquin Park, as well as Guelph University, Guelph, Ontario (with Steve Marshall and some of his laboratory at the time), and Memorial University, Newfoundland, were critical for the findings brought together here, and we acknowledge these institutions gratefully. All the coauthors sincerely appreciate the artistic hand of L.G.V., and for her diligence with the morphometric data analyses and assessments As the manuscript was revised and sent to press, we are moved to recognize and appreciate the significant contributions of R. W. (“Bob”) Lichtwardt, not only for his decades of research on and passion for the Trichomycetes but also as a respected teacher of mycology, mentor, colleague, and dear friend who helped instill such a strong desire to push forth and continue this legacy with an addictive desire to explore the world of arthropod gut fungi for generations to come.

Additional information

Funding

Funding from numerous agencies for and toward our various institutes and research programs has offered the opportunity to generate data over a number of years that have coalesced into this production, which is a contribution toward a broader and ongoing National Science Foundation (NSF) Collaborative Research effort deemed ZyGoLife. M.M.W. is very grateful to the ongoing support and generosity of Principal Investigator (PI) Jason Stajich (DEB-1441715), University of California Riverside. We also recognize former NSF awards BSR-8516581 plus DEB-7716161, -8019724, -9521811, -0344722, and -0108110 as well as collaborative awards DEB-0918182 and -0918169 to R.W.L. and M.M.W. for the role they played in allowing us to voucher specimen slides and DNA for longer-term examination and comparisons. L.G.V. is grateful for support from the Ministry of Science and Innovation (MICINN) of Spain for project number CGL2009-07141, also referred to as EUROTRIC-I. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation.