Diatom of the Month July 2019

Phylogeny matters: Applying the tools of ecophylogenetics to diatoms

by Francois Keck^1,2

Last year, like many other early-career diatomists, I was attending the International Diatom Symposium in Berlin. During our free time we had the opportunity to visit the greenhouses of the botanical garden. While looking at vascular plants, I am always amazed by the immense diversity of traits and strategies they have developed in the course of evolution. Back at the conference, there was no doubt that diatoms were not to be outdone in terms of their morphological and functional diversity. Traits in diatoms are incredibly diverse but their role in diatom ecology is very poorly known. Yet, this information is central for understanding biodiversity patterns in diatoms, and ultimately the factors driving community assembly in a clade of ca. 100 000 extant species.

In order to progress in the study of diatom ecology it is necessary to take into account the subtle differences between species and to move forward from the traditional approaches that treat species as equivalent morphological units. One way to do this is to integrate phylogeny, or the history of lineages, into biodiversity analyses. The idea that the evolutionary history of the species has direct consequences on community assembly mechanisms is at least as old as Darwin’s seminal theory of natural selection. If two species have diverged recently, they are more likely to share similar functional traits, and thus more likely to be influenced by similar environmental conditions. Moreover, the fact that closely related species have similar niche dimensions also implies some overlap with resources and competitors in a shared ecological space (Hutchinson, 1957). Hence, the evolutionary distance separating two species can serve as a proxy for species functional differences. Of course, there are many exceptions to this rule, but the idea is attractive and has gained large popularity among ecologists in recent years. About twenty years ago, Webb (2000) proposed an interesting statistical framework that combines phylogenetic information and ecological data to test whether species in communities are more related than expected by chance. He applied this framework to study tree assemblages in the Bornean rain forest, an ecosystem with very high species diversity (Figure 1). Webb's approach can provide important insights into the ecological processes that structure community composition (environmental filtering vs. competitive interaction) and has laid the foundations for the field of modern ecophylogenetics. However, these approaches were rarely applied to diatoms, possibly because large-scale reference phylogenies were lacking.

Figure 1: Two very different kinds of “forests”. Left: A tropical rain forest in Indonesia, where Webb applied his phylogenetic framework in the first place. Right: Artist's view of a microbial diatom biofilm. Interestingly, we can use a similar approach to study these two systems. In ecology, questions and methods can be transposed among scales and habitats. Left picture by Tom (license CC BY-SA). Right picture by Martyn Kelly. This image is part of an exhibition hosted by the Meise Botanic Garden and is reproduced with the author’s permission.

During my PhD at INRA (Institut National de la Recherche Agronomique) in France, I demonstrated the statistical links existing between freshwater diatom ecological preferences and their position in the phylogenetic tree. Here I would like to elaborate on the results we obtained during my stay in Sweden where I worked as a postdoc with Dr Maria Kahlert. We followed Webb’s approach and examined phylogenetic diversity patterns in freshwater benthic diatoms and their relation with the environment. To do this, we used a large dataset of stream benthic diatom communities sampled across Sweden (Figure 2) and the phylogenetic reconstruction of diatoms proposed by Nakov et al. (2018). We found that diatom communities were phylogenetically clustered, i.e., species within communities were statistically more closely related than expected by chance. This pattern is common in nature and is often interpreted as evidence for environmental filtering, i.e., local environmental conditions select against certain species. Another interesting result was that phylogenetic clustering was stronger in nutrient-poor environments where environmental conditions are expected to be more selective. More details and results can be found in an article that will be published shortly.

Figure 2. The Dalälven river, Sweden. Picture by Balticman, (CC BY-SA).

The purpose of this short post is to draw the attention of the young - and less young - diatomists to the field of ecophylogenetics. Species habitat preferences and interactions are the result of millions of years of evolution and we should take them into account when investigating mechanisms of diatom community assembly. With recent developments in molecular biology, the strong interest of diatomists in genetic studies and metabarcoding, and the publicly available databases such as GenBank, the volume of data for phylogenetic reconstruction is exploding. The latest phylogenies include more than a thousand species (e.g. Nakov et al. 2018), and this number is expected to continue to grow in the coming years as new research projects develop. This is exciting and will open the way for better comprehension of the link between phylogeny and ecology in diatoms. As an ecologist struggling to understand why there are so many species of diatoms and how diversity of assemblages is generated and maintained in nature, I am very excited by these future applications.

¹ Swedish University of Agricultural Sciences, Department of Aquatic Sciences and Assessment, Uppsala, Sweden

² INRA – UMR Carrtel, FR–74200 Thonon–les–Bains, France

References

Hutchinson, G. E. (1957). Cold spring harbor symposium on quantitative biology. Concluding Remarks, 22, 415–427.

Webb, C. O. (2000). Exploring the Phylogenetic Structure of Ecological Communities: An Example for Rain Forest Trees. The American Naturalist 156, 145–155. doi:10.1086/303378.

Nakov, T., Beaulieu, J. M., and Alverson, A. J. (2018). Accelerated diversification is related to life history and locomotion in a hyperdiverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta). New Phytologist 219, 462–473. doi:10.1111/nph.15137.

Keck, F. and Kahlert, M. Community phylogenetic structure reveals the imprint of neutral dynamics and environmental filtering by nutrient availability in freshwater diatoms. Accepted for publication in Scientific Reports.