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Bridging MICroevolution and MACroevolution in sticklebacks

Periodic Reporting for period 1 - MICMAC (Bridging MICroevolution and MACroevolution in sticklebacks)

Reporting period: 2019-09-01 to 2021-08-31

The MICMAC project aimed at better understanding the emergence of biodiversity by studying the links between microevolutionary mechanisms (at the population level) and macroevolutionary patterns (at the species level). Those two scales are often studied by different communities of researchers, using different tools and this is a major problem to study the evolutionary process as a continuum. A major goal of the project was study the link between those two scales, both theoretically (using models and simulations) and empirically with fishes as a model system (three-spined sticklebacks at microevolutionary scale and other species of fish at the macroevolutionary scale). I performed the research in the Schluter lab at the University of British Columbia in Canada during 17 months to build a general framework that could permit to understand how evolution unfolds from shallow to deep time scales. This work lead to the publication of 3 articles in high impact journal, and the organization of a workshop on the link between micro- to macroevolution. I have also generated a unique dataset with ~650 whole genome sequences across the Pacific and the Atlantic oceans for future work on stickleback evolution.
Since September 2019, I have published articles in high impact factor journals related to the project (Nature Communications, Molecular Biology and Evolution, Systematic Biology). These articles concern mostly the understanding of the pattern of fish biodiversity at the macroevolutionary level (WP2) and the link between microevolution and macroevolution (WP3).

The first of this article, published in Nature Communications, test a major hypothesis explaining the largest pattern of fish biodiversity on earth: the increase of diversity close the equator, also called the latitudinal diversity gradient. Many studies have proposed that stronger biotic interactions close to equator (such as predation) should be a major factor explaining why diversity is higher in the tropics. Using 55 years of fisheries data, we show that predation is higher in the temperate regions and not in the tropics, which was unknown before. This article received considerable media attention (Science daily, Forbes, New Scientist, …).

The second major article proposes to make a link between the composition of the genome of fish species and their vulnerability. Using a large genome data set of 76 species (including the three-spined stickleback), we show that vulnerable species accumulate more deleterious mutations than non-threatened ones. This is likely related to the fact that species with small population size experience weaker purifying selection, resulting in an accumulation of deleterious mutations. This article published in Molecular Biology and Evolution is key for all parts of the project, as it study fishes at higher taxa level and test the impact of microevolutionary dynamics (effective population size estimated from dN/dS) on a macroevolutionary event (extinction). It is thus an important step in the understanding of the interactions between micro and macroevolutionary scales (WP3). In parallel, I have participated to an article published in Systematic Biology using individual-based simulations to understand morphological evolution during speciation. This article showed that we must account for intraspecific variation when modelling morphological evolution during speciation, and this calls for more empirical studies linking micro and macroevolution.

In 2019, I obtained a grant to organize a working group and invite 17 renown researchers to the University of British Columbia (WP4). This workshop permitted to describe the potential links between micro- and macroevolution and the avenues worth investigating in the next years. It is a start for a new community of collaborators focusing on this emergent field of research as 6 other articles are in preparation related to this workshop (among them a key review in the field, WP3). In the same thematic, I was also invited to another workshop lead by R. Germain (UBC) focusing on the microevolutionary forces leading to speciation.

Much of the ongoing work of the project concerns the analysis of whole genomes for ~600 individuals of three-spined sticklebacks on a latitudinal gradient from California to Alaska and the sequencing of whole genome for ~50 individuals on a latitudinal gradient in Europe currently (sequencing done in Jan-Feb 2021). These new datasets should permit to understand what are the environmental and geographical factors determining the divergence between populations in sticklebacks (WP1). I have also learnt many technics of genomic analyses (DN/DS using PAML, STRUCTURE, ADMIXTURE, PLINK, BAYENV) and this was the main goal of this outgoing phase. Our preliminary results show some potential adaptations to latitude in Pacific, and we will use the samples from Europe as an independent latitudinal gradient to disentangle adaptation from neutral processes. I also plan to compare those results with whole-genomes of chinook salmon, sequenced in the lab and sampled on the same latitudinal gradient on the Pacific coast in order to detect whether the mechanisms of adaptation are also shared between divergent species. This comparison should indicates whether mechanisms of adaptation at the intraspecific scale (microevolution), are also important at a interspecific scale (macroevolution), as salmons and sticklebacks have diverged since more than 200 Millions years.
As a researcher, the main outcome of this project is that I obtained a permanent position at the CNRS (Centre National de la Recherche Scientifique) in France, starting in February 1st, 2021. As originally planned, the work done during this outgoing phase gave me the tools, datasets and an international community of collaborators to start my research in Europe and build a new team in the best conditions. The links between micro and macroevolution are complex, and I am excited to start a career on this thematic. On a short term, the next months will be focused on finalizing the review article from the working group, which should be a milestone in this research field. I will in parallel finish the ongoing analyses at the microevolutionary level (WP1). The final sequences are still currently being generated and we are waiting to have the whole dataset to share everything on NCBI. I will continue to work with D. Schluter’s network of collaborators to build a phylogeny of the gasterosteidae family using genomic data (K. Peichel, J. Merila, J. Kitano, WP2). Those analyses should be published in high impact journals and have a wide impact in the scientific community. On a longer term, my hope is that this research stimulates the public interest in evolution and the forces generating biodiversity
Potential links between micro and macroevolution