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What is a “species” for mycologists?

Updated: May 29, 2023

Prologue

The latest Asian Mycological Congress (AMC2021) was hosted by National Center for Genetic Engineering and Biotechnology (BIOTEC) at Science Park Convention Center, in Pathum Thai Thailand, from 3rd to 5th August 2022 (https://www.amc-2021.org/). I had an opportunity to present a talk entitled “Population Genomics at The Service of Fungal Taxonomy”.

At first, I wanted to do the talk to present my recent work on how I used population genomics to discover cryptic species and contribute to an improvement of fungal taxonomy. In a previous international seminar organized under a H2020 RISE program in which BIOTEC was involved, I already presented my work on the population genomics and the “integrative” taxonomy of some Beauveria species complexes (The presentation can be found here: https://www.researchgate.net/publication/359437850_The_Integrative_Taxonomy_of_Beauveria_asiatica_and_Beauveria_bassiana/stats). I felt like there was not going to be many new elements added for the new presentation as meanwhile I’d just started working on another fungal group and the data obtained were still preliminary. At the end, I felt that I was just going to showcase how my genomic data allowed the discovery of clear genetic differentiation between populations associated with variable difference in morphology and host association.

Something struck me...my principal work just consists of contributing to name new species by trying to relate more information from genomics. But...what is the purpose of my scientific work? Shall I be just satisfied of being able to have publications? to give new fancy species names? or to be recognized as someone who “discovers” these species of which I contributed to the knowledge dissemination?

As a biologist who had a general training in evolutionary biology with a specialized training in empirical population genetics and molecular phylogenetics, I’ve realized that my work was not about evolution; it was just about naming and categorizing. This realization reminded me of a question I had when I started my work at BIOTEC–what is a “species” for mycologists, and for fungal taxonomists particularly? That was the start of a personal and intellectual reflection that led me to make the recent presentation at the AMC2021 and to write this post eventually.

For doing my talk, I had this crazy idea to ask participants of the congress to answer to an online questionnaire about what a species is to them, how they decide whether some specimens should be considered as “new species”, based on what evidence either in the framework of phylogenetics or biological species concepts. I want to integrate the answers obtained to my presentation and discuss how population genomics used in (fungal) taxonomy is inscribed in a historical perspective of the taxonomic science; why it is useful and can be not only just an approach to help naming and categorizing, but also to dig into what all biologists working on biodiversity should ask themselves–How have the species we study emerged? As Mayr said “Nothing makes sense in biology except in the light of evolution”. What is the purpose of giving names to groups of organisms, based on variable criteria without understanding the force shaping the features of these criteria to diverge?


The survey

Background of the answerers

To know about the background of the participants in relation to the field of fungal systematics and taxonomy. Three questions were asked.


Question: Are your works related to the field of systematics and taxonomy of fungi?

Question: Are you actively working on the systematics and taxonomy of fungi?

Question: Do you consider yourself as a “taxonomist”?

From the pie charts shown above, we can conclude that most of the answerers work in relation to the fungal taxonomy, half work actively while only a minority consider themselves as a “taxonomist”. By focusing on those working actively in this field, only half (8 out of 16) consider themselves as taxonomist...

Something occurred to me here...most of us work in the field of fungal taxonomy, but many of us might do not feel fit to be called taxonomist...Why? Is it enough for me to call myself a taxonomist just because I published new species? Is it because some are just happy to be able to name something that interest them in other aspects beside the taxonomy such as–finding new secondary metabolites and bioactive compounds, developing relevant industrial and agricultural properties, etc.–and just don’t really care about the approach used to name and identify species? Are we really sure about what we do exactly? What is a “species” exactly? What should be the “absolute” criteria for naming new species?


Definition

My questionnaire started by asking the participants to define what a “species” is according to their perception.


Question: Give the definition of a "species" according to your personal understanding.

By collecting 30 answers to this question, I did a word frequency analysis by removing the word “species” from the answers because the question was about defining this word itself, making it redundant and hindering the weight of other words used to explain the perception of the word “species”.

This words cloud summarizes the results from the analysis. The most frequently used words were such “group”, “individuals”, “organisms”, “similar”, “different”. Overall, the results gave a general idea that a species should be a group of organisms that are similar enough to be the same species, and different enough from other groups to be viewed as different species. This is not new; it is almost common sense for us all human observing the living world outside! What are similar should be the same species, and what are different should be just different species, right?

Less cited but still quite frequent words were “characteristics”, “characters”, “exchanging”, “isolated”, “genetic”, “interbreeding”, “fertile”. This gives the idea about different operational criteria that could be used for distinguishing or delineating species. To my opinion, these words can correspond to two operational species concepts, the morphological species concepts (MSC) and the biological species concept (BSC).

What struck me here the most was that words such as “phylogeny”, “phylogenies” or “phylogenetic” were practically not cited while the phylogenetics species concept (PSC) seems to be predominant in mycology!


Only one answer from the 30 received mentioned the word “phylogenetic”:


“Alongside 30+ known definitions I have seen I think Darwin said it was 'defining the undefinable'. For sympatric sexual taxa I consider species should be reproductively isolated. Among asexual and allopatric taxa I would mostly consider phylogenetic distance and notable phenotypic distinction.”


To me, this might be the most elaborated and complete answer received from the entire survey.


Still, what was quite interesting to me was that there was no mention of the word “speciation” in none of the answers. But to be fair, I asked the participants to define the word “species”, not to explain how the species emerged. But even though, most of mycologists are not interested to understand how the species we study did emerge.


The integrative taxonomy and the various species concepts.

The answers to the definition of the word “species” suggested that different people used different criteria to consider a taxon as a species. But there is one evident consensus, most of us think that it is necessary to refer to several species concepts when working in fungal taxonomy.


Question: Is it important to refer to several species concepts when working in fungal taxonomy?


Integrating several species concepts to designate new species is a scientific approach called “Integrative Taxonomy”. This term was first proposed by zoologists (1,2). A few authors did try to define it. We can summarize that the integrative taxonomy is a synthesis between different criteria to delineate species, thus referring to various species concept. But how do we integrate these different criteria? Are we, as mycologists, familiar enough with the various species concepts out there? Or are we just repeating some patterns we are more familiar with? Where are we exactly in the 21st century when the technologies have been so advanced and allowed generating a tremendous amount of genomic or high-throughput data.


The species problem

To place all these interrogations into their context, I think it is best to first ask what the “species problem” is. What kind of questions can we ask related to the word “species”? Richards (2010) (3) proposed that questions related to the species problems can to be classified into three categories:


1) “What is a species?” in terms of theory and concepts.

As a theoretical concept, is species a reality? For example, if in mathematics we say 1+1 = 2; it is undeniable. But with “species”, does this word have extramental significance outside our human mind? To debate on this matter, it would take so much deepened philosophical reflection that I’m not dare enough to handle here. On the other hand, as an operational concept, this problem deals with the different species concepts and debates on the legitimacy of one another.


2) “How to distinguish and recognize species?”

This problem deals directly with how the taxonomists practically designate new species, and most of the taxonomic work in Fungi are situated at this level.


3) “What is the origin of species?”

This question led to the study of “speciation”, or an ensemble of mechanisms generating species diversity. The answers gathered from my survey showed that mycologists mostly perceived the species problems only for the second issue. This is also reflected in the amount of related literature. So, just to show you how limited is the “taxonomic” works done by mycologists, I search the Web of Science on 6 October 2022 with different keywords in relation to these different categories of problems.


For the 1st category, with the keywords: Fungi, New Species, Species Concept. We found 481 publications from 2001 to 2022.

For the 2nd category, with the keywords: Fungi, New Species. That means it include all work related to the study of naming assigning new species without any particular focus on other aspects of the species problem. We have 19,924 publications for the last 22 years.  901 publications per year.

For the last category related to the study of speciation, with the keywords: Fungi, New Species and Speciation. We have only 324 publications for the last 22 years, with 15 publications per year.


This means...


“Most of the taxonomists limit themselves to circumscribing new species without reflecting on different concepts or deepen the understanding on the origin of species!”


The species concepts

So, let’s just focus on what interest the taxonomists most, which is naming new species. Which species concept do they use the most?


By referring to the most used species concepts (4) which are as follows:

- “Phylogenetic species concept” = based on monophyly with strong support and/or concordance among markers.

- “Biological species concept” = based on reproductive isolation and interbreeding with viable offsprings.

- “Morphological species concept” = based on morphological similarity and dissimilarity.

- “Ecological species concept” = based on shared ecological niches


We can see that most taxonomic works refer to Phylogenetic Species Concept with 250 publications found using the keywords: Fungi, New Species, Phylogenetic Species Concept. The 2nd is the morphological species concept with 187 publications. Then comes the “biological species concept” with only 81 publications. Finally, only 41 publications with the “ecological species concept” even though all fungal taxonomists seem to agree that different species should occupy different ecological niches, but apparently not many people really materialize this thought into their taxonomic work.


Phylogenetic Species Concepts

Although the “phylogenetic species concept” seem to the most predominant among mycologists, not everyone agrees on how to apply this concept. Basically, the phylogenetic species concept is generally materialized based on the monophyly with strong supports of a clade. But how do we consider the “support” diverge between those taking the strong bootstrap of a concatenated-genes tree and those taking the concordance between different loci supporting the clade. While the monophyly of concatenated-genes tree has become a common ground for fungal taxonomic works, Taylor et al. (2000) who had laid the foundation of the modern interpretation of this species concept clearly sees the concordance as a more reliable approach to support a clade. And (not so?) surprisingly, when the question of whether the strongly supported monophyly from a concatenated-genes tree is more important than the high concordance between gene trees, more participants think that the most important criterion to delimit species is the strongly supported monophyly. When they were asked what to chose between two conflicting trees, one with strongly supported monophyly and another with highly concordant clade, the majority answered the would chose the former and not the latter.


Question: What is the most important criterion to delimit a species according to the phylogenetic species concept?

Question: If there is a strongly supported monophyly but with a low concordance between markers, or vice-versa, what would you choose as the definitive criterion to delimit new species?

Epilogue

What can I say? Will there be one day a unifying concept that makes all taxonomists agree together with highly efficient criterion? Or we will have to rely on permanent debates and moving consensus? To solve these problems, it is not enough for the taxonomists to name new species with nice pictures but to really dig into the philosophical foundation of the taxonomy. I surely don’t have solutions. But I just want to shout out to my fellow researchers in taxonomy of fungi that:

- Taxonomy is a tool for communication established based on variably objective criteria,

- A species is just a hypothesis. It is not to be taken for granted.

- We need to connect different species concepts as a basis to understand how the species emerge, and not just to categorize living organisms.

- We should look at the frontier of different species concepts. This would potentially lead to the understanding of speciation.

- Always try to see the whole picture of the living world, not just to make new names for biological organisms that interest you!




References

1. Dayrat, B. Towards integrative taxonomy. Biol. J. Linn. Soc. 85, 407–415 (2005).

2. Will, K. W., Mishler, B. D. & Wheeler, Q. D. The perils of DNA barcoding and the need for integrative taxonomy. Syst. Biol. 54, 844–851 (2005).

3. R. A. Richards, The Species Problem (Cambridge University Press, 2010; https://www.cambrid- ge.org/core/product/identifier/9780511762222/type/book)

4. Stengel, A., Stanke, K. M., Quattrone, A. C. & Herr, J. R. Improving Taxonomic Delimitation of Fungal Species in the Age of Genomics and Phenomics. Front. Microbiol. 13, (2022).

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