The Dentinger Laboratory at the Utah Museum of Natural History has published a provocative new article in the journal New Phytologist that describes their work with the beloved fungus, edible mushrooms, better known to foodies around the world as porcini mushrooms. In the paper, Keaton Tremble and Bryn Dentinger, PhD, present a first-of-its-kind genetic study of porcini mushrooms in the northern hemisphere. By evaluating the genetic code of these samples from around the world, they learned that these delicious mushrooms evolved in surprising ways – contrary to the expectations of many who might think that geographic isolation would be the main driver of species diversity. In fact, there are regions in the world where ceps retain their genetic specificity in local ecological niches, even if they are not geographically isolated from other genetic lineages.
The French word land, made famous by winemakers, immediately comes to mind. Terroir describes all the local factors such as soil types, sunshine, degree of slope, microclimate, soil microorganisms, etc. that make each plot of land produce distinctive wines. It is a celebration of the local ecology and its impact on the vine, the grapes and the finished product. The new study by Tremble and Dentinger offers mushroom pickers tantalizing data to affirm that the porcini mushrooms from their secret forest express the qualities of their terroir in the same way as the best wines in the world.
But that is not the purpose of the study. With the advent of genetic sequencing, most genetic studies in mycology have focused on describing the unique characteristics of fungi in a small geographic area. Tremble and Dentinger wanted to do something different. Rather than simply comparing a group of mushrooms from Colorado to a group from California in order to call them different species, they wanted to better understand global trends in how the genetic code was preserved or modified in porcini mushrooms. “Our study is important because it goes beyond the overly simplistic sampling method used in the past,” says Dentinger.
What they discovered is that porcini mushrooms have evolved in different, yet clearly recognizable ways, across the world. “In North America, there is a strong stratification of distinct genetic populations in local areas, despite the fact that they are not reproductively isolated,” says Tremble. “Yet in Europe, there is a line that dominates from Spain to Georgia via Scandinavia.”
Evolutionary biologists generally believe that there is one evolutionary strategy that governs the process of speciation for a particular organism, but Tremble and Dentinger showed that ceps actually exhibit multiple and divergent strategies. In fact, this is the first genetic study in any organization show such a result on a global scale.
A related and significant finding is a refutation of the traditional notion that isolation is the primary means by which species develop their uniqueness. As the Encyclopedia of Ecology (Second Edition – 2019) proudly states: “All evolutionary biologists agree that geographic isolation is a common, if not the most common, mechanism by which new species arise (Futuyma, 2013 ).”
More than identifying mushrooms
It’s an exciting time to be a mycologist. Not only is the fungal kingdom barely explored and described, but DNA sequencing technology has introduced a seismic shift in how mycologists classify fungi. For millennia, humans have identified which mushrooms are good to eat from which are poisonous based on their appearance or phenotype. But phenotypes can be deceiving – think of a brother and sister who have different hair color, different nose shapes, etc. They are even more genetically similar to each other than to other people in the population. Thus, genetic similarities are seen as the true marker of different species, going against the trend of identifying fungi that dates back to the beginning of mankind.
In addition to this, let’s remember that fungi are only the reproductive structure of the main organism, called mycelium (see the illustration below, “Basics of fungi”). Like icebergs, the mycelia show us only the tip of themselves, while the massive fungal body lives underground, bound to the roots of trees. edible mushrooms spreads geographically thanks to the tiny spores released by porcini mushrooms, carried by the wind, mammals and even flies. Thus, biologists are tempted to believe that in any geographic area where spores can fly, a species will be defined by the genetic intermingling within that geographic space.
Tremble and Dentinger’s study strongly refutes this hypothesis.
In North America, different genetic lineages exist side by side, and despite genetic evidence for admixture, local ecological factors have played the greatest role in maintaining the distinctness of these lineages. “Utah happens to be one of the areas where two distinct bloodlines live,” Dentinger notes. What these lineages show is that local ecology is a more important factor in maintaining their genetic distinctiveness than gene flow from other lineages.
“This article shows that you don’t need isolation for genetic divergence,” says Tremble. “The force of ecological adaptation is so strong in edible mushrooms that while you can scatter spores virtually anywhere, there is strong selection to suit specific environments.
The wonders of dried porcini mushrooms
The secret of their study lies at the heart of natural history museums: mushroom collections. Tremble is a doctoral candidate at the School of Biological Sciences, defending his thesis in the spring of 2023 to receive his degree in evolutionary biology. He made a fortuitous choice in working with Dentinger as an advisor – as Curator of Mycology at NHMU, Dentinger established the NHMU Genomics Laboratory to be able to analyze DNA quickly and efficiently. More importantly for this study, Dentinger’s professional contacts in natural history museums around the world helped Tremble gain access to the 160 samples that otherwise would have been nearly impossible to collect.
“You have to rely on opportunistic encounters in the wild to collect a living sample,” says Dentinger. “It’s fundamentally different to work with plants, which are there every season, and animals, which you can bait.” Thus, it would have taken an incredible amount of logistics, timing, and luck to find, correctly identify, and ship 160 different samples across the northern hemisphere to the NHMU lab.
Instead, “our study was made possible by fungi,” says Dentinger, referring to the name of mushroom collections in museums. They plumbed the depths of NHMU’s fungarium and reached out to collaborators around the world.
“Without the fieldwork accumulated by 80 different people, this would not have been possible,” notes Tremble. All samples were dried ceps, stable and ready for Aspen to extract their DNA. Since edible mushrooms mycelia have a surprisingly long lifespan (estimated at 45 years), they only used samples dating back to 1950 to ensure that the study only looked at a few generations.
Aspen used sophisticated software to perform statistical analyzes on these samples. He genotyped 792,923 SNPs (pronounced “snips,” short for single nucleotide polymorphisms), which are the individual ways in which the 160 porcini genomes differed from each other. In order to classify major lineages, he filtered out SNPs that were only present in one sample (which would be considered a simple “family unit” or individual variant) so that only major differences between genomes could be observed. In the end, Tremble identified 6 main lineages.
By feeding his data into mathematical models, Tremble discovered a complex web of genomic mixing, where lineages remained distinct despite evidence that other lineages had mixed with them. Their modeling and geographic sampling data showed that this ability to remain distinct was due to environmental adaptation, not physical isolation.
Lineages or species?
Aspen and Dentinger take a decidedly agnostic approach to whether they should identify these 6 distinct lineages as “species”. They refrain from doing so in their paper because they want to focus on genetic data and broader questions related to strategies in evolutionary biology. Also, this species discussion is a controversial conversation.
“There is no formal process for defining a species,” notes Tremble, “it’s an ongoing debate. We didn’t want to call them species or subspecies, because that automatically implies that they are separately evolving groups, which they certainly aren’t. They decided to call them lineages because this term is genetically resolvable, i.e. lineages can be quantifiably distinguished from each other using statistical genetic approaches.
But that doesn’t mean they don’t want to tackle taxonomy. “It will be an article to appear in another journal,” says Dentinger. The mushroom world has never experienced the Victorian-era explosion of species identification and naming that occurred with animals and plants. With only about 5% of the diversity of fungi identified, naming and taxonomy must take place, if only to help mycologists talk about their subject.
However, the species-subspecies taxonomy for edible mushrooms shakes, Dentinger assures us of one thing: “Terroir is more important than people thought.”
So find a mushroom picker and get on his side to find the ceps best suited to your palate.
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