Les mécanismes des changements évolutifs et de l’adaptation / The mechanisms of evolutionary changes and adaptation

Séminaire FSER organisé par Nicolas Gompel (LMU Munich, Germany) et Benjamin Prud’homme (IBDM, Aix-Marseille Université, France) du 20 au 25 avril 2015

Participants

Wolfgang Enard, Nicolas Gompel, Ilona Grunwald Kadow, Alexander Johnson, Mathieu Joron, Artyom Kopp, Marie Manceau, Arnaud Martin, Virginie Orgogozo, Benjamin Prud’homme, Lluis Quintana-Murci, Paul Rainey, Mark Reibez, Ralph Sommer, Joseph Thornton, Miltos Tsiantis, Patricia Wittkopp

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Résumé

The objective of the seminar entitled ‘The mechanisms of evolutionary changes and adaptation’ was to bring together a variety of specialists to confront their views on the nature and the relative influence of the forces that sculpt the course of evolution. The seventeen participants presented their work focusing on particular aspects of evolutionary changes, dealing with different levels of biological organization (molecules, networks, cell, organs, organisms and populations). The different presentations can be split, sometimes a bit arbitrarily, into six major themes: Molecular evolution, Gene network evolution, Identifying genes involved in human evolution, Role of constraints and biases, Adaptation to different environments and Evolution of behavior.

The seminar enlightened several trends that emerged through the comparison of the different presentations and illustrated the necessity and the value to extend the interactions among various communities of biologists that address evolutionary questions from different perspectives and using various model systems.

Nota : cette rencontre a été à l’origine de la publication par Mark Rebeiz et Miltos Tsiantis de l’article « Enhancer evolution and the origins of morphological novelty »

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Compte-rendu

The six major themes of the meeting are detailed hereafter:

1. Molecular evolution

The most fundamental level of divergence between individuals and species lies in the composition and function of the molecules (mostly genes, and proteins coded by these genes) that constitute them. J. Thornton discussed how the sequence of a transcription factor protein evolved a novel function and DNA binding specificity by experimentally exploring the mutational landscape. Similarly, P. Wittkopp examined exhaustively the set of nucleotide changes that modify a particular gene expression. These presentations illustrated the thermodynamic constraints limiting protein evolution, and how selection limits the accumulation of noise in gene regulation.

2. Gene network evolution

Genes and proteins rarely act alone, but rather are parts of large interacting networks, and it is often more relevant to examine the evolution of entire networks than individual molecules. Several participants (A. Martin, N. Gompel, V. Orgogozo, M. Rebeiz, M. Tsiantis, A. Johnson, A. Kopp) studying yeast, plants, flies or butterflies, provided different examples of gene regulatory interaction evolution. We are now seeing in molecular terms, and with an unprecedented resolution, how these interactions take place and how they diverge across species. Remarkably, similar mechanistic trends are observed in organisms as different as yeast, animals and plants, suggesting common, and therefore general, underlying basis. Gene networks evolution really is a major contributor to the evolution of species.

3. Identifying genes involved in human evolution

Experimental approaches to study the genetic basis of human biology have always been challenging. Functional genomics approaches (presented by L. Quintana-Murci) and ‘humanized’ mouse models (used by W. Enard) allow to explore human biology and genetics. These approaches identify genes and mutations associated with human evolution, pertaining to resistance to diseases or the emergence of enhanced cognitive skills such as speech.

4. Role of constraints and biases

The production of particular novel variants within populations can be facilitated, or prevented, because of specific biases or constraints, respectively. These biases and constraints can operate at the genetic (or even genomic) level, or at the developmental level. M. Joron illustrated how chromosomal inversions including genes responsible for the formation of butterflies’ wing coloration patterns prevent recombination within this region and therefore maintain distinct color morphs in natural populations. In contrast, M. Manceau showed how developmental processes produce preformed landmarks that can be used as canvas to create novel coloration patterns.

5. Adaptation to different environments

Organisms can respond relatively quickly to changes in the environment in which they live. R. Sommer illustrated and dissected how nematode worms have evolved a plastic response to produce two types of morphs with different mouth architectures in response to different conditions. P. Rainey showed how multicellularity can quickly evolve, in bacteria, when ‘forced’ to cooperate to survive adverse conditions, offering a plausible scenario for metazoan evolution driven by ecological and selective pressures.

6. Evolution of behavior

The evolution of novel behaviors is still largely mysterious. Addressing this question certainly requires a profound understanding of neural circuits and the gene networks that build them and impart their function. I. Grunwald-Kadow illustrated how this understanding can help our understanding of the evolution of behaviors as essential as feeding and egg laying. In a complementary manner. B. Prud’homme explored the genetic and neuronal basis of an invasive pest fruit fly species that has evolved a novel egg laying preference.

In conclusion, this seminar enlightened several trends that emerged through the comparison of the different presentations. First, it’s becoming increasingly feasible to identify the genes and the changes in these genes involved in evolutionary divergence. In turn, this has revealed that the genetic route of evolutionary changes is somewhat predictable, following identifiable and understandable paths of least resistance, the one that produce a phenotypic modification with a minimal number of genetic changes. Second, the course of evolution is surprisingly repetitive, with similar transitions having occurred multiple times in response to similar environmental conditions. This amount of repeatability in evolution appears surprising, especially in the face of the seemingly endless diversity in the natural world.

The seminar illustrated the necessity and the value to extend the interactions among various communities of biologists that address evolutionary questions from different perspectives and using various model systems. Meetings such as this one are superb opportunities for this!