Research

My research covers many aspects of fish biology that converge to the theme of life in extreme and changing environmental conditions. Fish are amazing to study because they colonized almost every single aquatic habitat on the planet, from the surface to deep-sea trenches, from salt to fresh water, and from the heat of the tropics to the frigid temperatures of the poles. How did such an amazing diversity arise? What are the genetic, physiological, and evolutionary mechanisms that permitted such diversification and adaptation to extreme conditions?

Today, aquatic ecosystems face major risks. Global warming and human activities are altering our coasts and oceans at a magnitude never seen before. These perturbations can tip a species or an ecosystem from a healthy state to collapse. However, we have a limited understanding of the sensitivity of fish to ecological disturbance. We are therefore unable to predict how global warming and human activities will affect them and how to mitigate our impacts to preserve the existing biodiversity and the services it provides.

Understanding the evolutionary processes of adaptation to extreme conditions can help us discern the mechanisms of the resilience of life, and its limits, to reveal the capacity of today’s life to withstand predicted environmental changes and provide the scientific evidence necessary for motivated ecosystem management and conservation policies. My research thus aims at understanding the mechanisms by which fish evolved and adapted to hostile or changing environments, and questions how today’s fish withstand ongoing and predicted alterations to their environment.

To question the capacity of fish to adapt and evolve in extreme conditions, I study Antarctic fishes, fish reproduction and development, and the role of microRNAs in adaptation and evolution.

Antarctic fishes

Antarctic fishes are a fantastic group of fish to study adaptation and evolution in extreme conditions. How much more extreme than living in constantly freezing water all year long can you get if you’re a fish?! While most other fish disappeared from Antarctica as it cooled down starting 30 million years ago or so, one group of fish, the notothenioids, evolved the capacity to produce an antifreeze protein that allowed them not only to survive but to thrive in the frigid waters of Antarctica. Among this group of Antarctic fishes we can also find the truly unique white-blooded icefishes, the only vertebrates living without hemoglobin. Their blood is opalescent white compared to the dark red color of our blood or of any other vertebrate. How did that happen? How did they adapt following the loss of hemoglobin? Is this exceptional biodiversity at risk with climate change? This is a key question because adaptation to constant cold turned out to be a double-edged sword: Antarctic fish are now unable to cope with warmer waters. However, a few groups of Antarctic notothenioid fish managed, at a few occasions over millions of years, to escape the harsh Antarctic conditions and to re-adapt to more temperate waters around sub-Antarctic islands and Patagonia. How did their ancestor do that? Would today’s species be able to evolve similar or alternative mechanisms to face predicted climate change that is affecting the poles at a pace faster than at any other place on the planet?

Because of the specifically remote, harsh, and rarely accessible nature of Antarctica and thus the collective scientific value of each specimen and data collected, my work on this continent is fundamentally transdisciplinary, international, and highly collaborative. This drives me to a wide array of research questions that include:

• What genetic and physiological mechanisms accompanied acclimation to cold? How did species re-acclimate to temperate waters?

• How did Antarctic notothenioid species diversify? Was reproductive isolation a driving factor in species evolution?

• How did globin genes evolve in Antarctic fish and in white-blooded icefishes? How do icefishes survive without hemoglobin?

• What are the physical and biological threats that Antarctic fish face? Will they be able to cope with those threats and new ones?

The role of microRNAs in adaptation and evolution

I am also interested in the yet incompletely understood role of microRNAs in adaptation and evolution. MicroRNAs (miRNAs) are small non-coding RNAs that regulate protein-coding gene expression by binding to the tail (3’UTR) of messenger RNAs when a miRNA gets incorporated into the RNA-induced silencing complex (RISC). In other words, miRNAs can reduce the expression of specific genes in specific conditions. In animals, miRNAs are implicated in virtually every biological process, including cell proliferation and differentiation, development, physiology, and pathologies. In addition, miRNAs are thought to provide robustness to embryonic development by buffering genetic noise, especially in stressful conditions, which contributes to phenotypic canalization. Conversely, miRNAs are also hypothesized to promote the emergence of new phenotypes by differentially modulating developmental and physiological pathways, which can influence adaptation, diversification and speciation.

• How did miRNAs evolve in fish? Did some species lose important miRNA genes or evolve new ones? What are the genetic factors that influence miRNA gene evolution?

• Was the evolution of miRNA genes in numbers, sequences, and expression patterns related to events such as whole genome duplication or adaptation to changing or novel environments?

• How do miRNAs contribute to adaptation and evolution by modulating gene expression?

To answer these questions, I lead the development of a bioinformatic tool, Prost!, that analyzes small RNA transcriptomic data produced on sequencing machines such as Illumina. I also collaborated with researchers from 14 institutions and five countries to develop a novel standard miRNA-seq file format, miRGFF3, facilitating downstream analyses. And using these tools I annotated miRNA genes and their products in more than ten species of fish and analyzed their contributions to ecological adaptation, control of reproduction and development, and species evolution. In collaboration with INRA in France, we have recently developed a novel miRNA database: FishmiRNA: An evolutionarily supported microRNA annotation and expression database for ray-finned fishes. Many more studies are also ongoing to understand the role of these elusive RNAs!

Fish reproduction and development

Reproduction is essential to propagate life and is an important driver of evolution. I am interested in fish reproduction on many aspects from sex determination mechanisms, progression of gamete formation and its cycles, hybridization and the mechanisms preventing it, to the role of specific candidate genes, including miRNAs, in these contexts. Because reproduction is immediately followed by the development of an embryo, a larvae, and then of a juvenile fish, I am also studying fish early development with a particular interest for skeletal development because bones define the shape fish will have and the movements it will be able to do.

• What are the modalities of Antarctic fish reproduction? From sexual determination, annual reproductive cycles, to the role of reproduction and hybridization in species individualization.

• How do Antarctic fish embryos develop? How is their development changing under different environmental conditions?

• How did the fish skeleton evolve over hundreds of millions of years? With a special interest on the fish tail, the caudal fin, which used to be asymmetrical like in sharks and in the paddlefish (see picture on the left) but became symmetrical in most fishes about 300 millions years ago.

• What molecular mechanisms drive the coordinated development of the caudal fin skeleton in fish? For this I take advantage of the laboratory model species zebrafish in which many transgenic lines enable us to question development of various cell types, tissues, and organs?

• What is the role of miRNAs in embryonic and larval development in fish?