Understanding evolvability

Evolvability is the ability of living organisms to evolve. On the short term, evolvability depends on the presence of heritable (genetic) variation. On slightly longer terms, evolvability depends on the ability of organisms to produce and maintain such potentially adaptive genetic variation and thus on the ability of developmental processes to translate molecular variation into phenotypic variation. Consequently, evolvability is mostly affected by the structure and properties of the development. This view that emerged in the 90´s contrasts with the classic view in quantitative and population genetics where genetic variation was considered as granted and variation in the potential to evolve was mostly attributed to selection, that is, processes external to the organism. In such paradigm, evolvability was not considered as a topic of research. Unfortunately, the use of heritability where genetic variance is scaled by the total phenotypic variance for comparing of evolutionary potential across traits and populations also hampered progress in the study of evolvability, because it confounded changes in genetic variance with changes in the other sources of phenotypic variation. Building on Houle (1992, Genetics), the two PIs of this project have suggested that mean-scaling of genetic variance (mean-scale evolvability) offers a better metric to compare the evolutionary potential across traits and populations and to study the consequence of evolvability on macro-evolution, that is, evolution above the population level. In this project, using mean-scaled evolvability we aimed at better understanding variation in short-term potential for evolution and its consequences on patterns of divergence between populations and species. By reviewing the literature and reanalysing published data, we have shown that many previous predictions concerning the effects of selection, population size and environmental variation on the potential to evolve were not supported. This likely stems from the fact that variation in short-term evolvability is mostly due to changes in allelic effects more than changes in allele frequency. Building on previous work by one of the PI (TFH), we further developed a new statistical framework to quantify systematic changes in allelic effects, and therefore evolvability, with changes in the trait mean. Using this new framework to reanalyse published data, we have shown that such effects, referred to as directional epistasis, are prevalent even in simple morphological traits. We have also shown that evolvability affects evolutionary divergence among populations, and to a lesser extent among species. Combining different data sets with complementary strength, we have evaluated and rejected several hypotheses to explain this relationship between evolvability and divergence, and we proposed that this relationship results from the influence of genetic constraints on the ability of populations to track rapid, stationary environmental fluctuations. The project has resulted in the publication of nine articles in leading journals in evolutionary biology as well as 5 book chapters that are part of a book on Evolvability edited by the two PIs. One post-doc and one PhD student (PhD defense planned in November 2024) have been employed on the project.

One of the main goals of our research on evolvability for the past 20 years has been to advocate a measurement of the ability to evolve that is firmly grounded in the measurement theory. This measure, the mean-scaled evolvability, has been developed for the specific purpose of better understanding variation in the potential to evolve across traits, populations and species, and its evolution. The main goal of our project was therefore to promote this “new” measure of evolvability by explaining it and showing its explanatory and predictive values for understanding evolution at different timescales. With the publication of a review paper in one of the most prestigious book series in ecology and evolution (Annual Review in Ecology, Evolution and Systematics) and the publication of an edited volume about Evolvability, we believe that our perspective on this subject will reach a broader audience. We already got feedback from some of our colleagues that are using our book for post-graduate classes. Other publications that came out of this project have been also published in leading journals in evolutionary biology (Evolution, Evolution letters) or in very high impact generalist journals (Proceeding of the National Academy of Science, USA). We therefore expect that our perspective will become more broadly accepted following this project. We also expect that our project, by providing clear examples on how measurement theory can be used to derive tools for quantifying properties of biological entities will help the development of better and more meaningful metrics in quantitative ecology and evolution.

Evolvability is the ability of organisms to respond to selection. This concept is central to many questions regarding the ability of species to adapt. On short time-scales, evolvability depends on the amount of additive genetic variance. Yet, evolvability, variation in evolvability and the factors responsible for this variation are poorly understood. To improve our understanding on evolvability, we will synthesize the empirical knowledge on additive genetic variance and identify the key factors affecting this property of living organism. To achieve this, we will explore the contribution of species characteristics, traits genetic architecture and environmental factors affecting evolvability. These analyses will be performed using novel statistical tools developed by the research team.