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Evolution of the thermal plasticity of gene expression: a reverse evolution experiment using Drosophila simulans.

Periodic Reporting for period 1 - ReversePlasticity (Evolution of the thermal plasticity of gene expression: a reverse evolution experiment using Drosophila simulans.)

Reporting period: 2015-04-01 to 2017-03-31

Phenotypic plasticity, the ability of a genotype to express distinct phenotypes in different environments, is assumed to facilitate individuals coping with new or rapidly changing environments. In the context of climate change, the phenotypic response to temperature has received particular attention since thermal plasticity is affecting the survival of populations and species distribution. Although temperature is an important variable that affects many traits, the genetic basis of phenotypic plasticity evolution remains poorly explored.

Temperature does not only affect integrated components of phenotype such as physiology or behaviour but also gene expression. Indeed, the concept of phenotypic plasticity was originally conceived for phenotypes but it can be also applied to patterns of gene expression or protein profiles. Understanding how adaptive plasticity is evolving in populations exposed to new environments could provide insights into the mechanisms driving gene expression temperature sensitivity as well as its molecular basis.

Experimental evolution is a highly promising approach to study adaptation, as this research tool controls for the environment and the population history and allows for replication. An innovative way of characterizing the evolution of adaptive plasticity is to monitor gene expression patterns after evolution in stressful or novel environments during experimental evolution studies. The pattern of gene expression change across a range of environments can be defined as the reaction norm of the molecular phenotype of these populations. With the development of Next Generation Sequencing (NGS), it is now possible to identify changes in gene expression and the associated reaction norms during evolution.

The objectives of our project were to study the interplay between phenotypic plasticity and genetic evolution during adaptation to novel thermal environments:
- Is phenotypic plasticity in natural population adaptive?
- Does adaptive phenotypic plasticity prevent genetic evolution? Facilitates it?
- Can we identify genomic regions rapidly evolving in response to temperature changes and how these changes affect phenotypic plasticity?

Our research demonstrated that the evolution of phenotypic plasticity is involved during adaptation to novel thermal environment. We showed that natural populations exhibit genetic variation for plasticity that can rapidly evolve in laboratory experiments. We then identified the genetic regions associated with these phenotypic changes and described their evolution. Because these genes also show pronounced clinal variations in natural populations, we conclude that similar processes drive rapid temperature adaptation in the wild.
This project relies on a selection experiment with Drosophila simulans populations that evolve in one of two different thermal environments (hot, fluctuating between 18 and 28°C and cold, fluctuating between 10 and 20°C). From this work, we derived multiple experiments in order to investigate the genetic and phenotypic changes occurring during evolution. First, we designed a “reverse selection” experiment: flies that initially were selected in our cold treatment were then shifted after four years to the other environment. Then, using common garden experiments we analyzed the gene expression profiles of evolved populations and contrast them with their ancestral value. In parallel, we investigated rapid genomic changes in the main experiment in order to link phenotypic changes to genetic target of selection using NGS technologies.

We showed that phenotypic plasticity of gene expression in a natural population of Drosophila simulans was evolving during adaptation in novel thermal environments and managed to explore some of the molecular basis of its rapid evolution. In particular, we demonstrated that:

- Selection in hot environments led to rapid changes in the metabolism regulation of the fruit flies, leading to profound changes of gene expression associated with the main biological pathways involved in energy production

- Phenotypic evolution relies on the evolution of phenotypic plasticity and not on constitutive changes (independent of the temperature).

- Phenotypic plasticity in the ancestral populations is adaptive: the direction of evolution in experiment is in the same direction than the ancestral plasticity. This suggests that selection for thermal plasticity occurs in natural populations, potentially due to seasonal and local variations

- These complex phenotypic changes rely on a simple genetic basis. We identified two evolving genes involved in the activity of a single enzyme, the AMP-Kinase, a key regulator of cellular homeostasis. Contrary to theoretical expectations, complex phenotypic traits can evolve rapidly due to changes in frequency of a small number of genomic regions, each having an important impact on the phenotype.

- The same genetic regions show pronounced latitudinal variations in North America, demonstrating that replicated laboratory experiments are well-suited to dissect and functionally characterize adaptive processes relevant to natural populations.

These results have been presented at two international conferences during the duration of the project and led to two research manuscripts that will rapidly be published.
Our work provided an experimental demonstration that phenotypic plasticity of Drosophila populations can evolve when submitted to a more extreme temperature than encountered in their native environment. We described phenotypic changes associated with these adaptations that could help understanding how species and populations can respond to rapid temperature variations, such as human induced climate change. Our results open new research question, suggesting an important role of cis-regulatory genomic regions in the evolution of temperature dependent regulation of gene expression and especially in the way phenotypic plasticity allows populations to deal with rapid temperature changes.

Additionally, we identified one specific enzyme, AMPK, which central role in metabolic regulation and metabolic disorders, have been identified in numerous species, including in human. We believe that studying its role in adaptation to different thermal environment could shed a new light on the function of its numerous isoforms.