Skip to main content

The molecular process and functional consequences of adaptation

Final Report Summary - ADAPT_EVOL (The molecular process and functional consequences of adaptation)

Adaptation is the key concept in Evolutionary Biology. Understanding adaptation has important implications for basic and applied science since adaptation underlies processes such as the ability of species to survive in changing environments, resistance to antibiotics and cancer chemotherapies, and host-pathogen interactions. The recent increase in availability of whole genome sequences makes it possible to search for evidence of adaptation at an unprecedented scale. However, current approaches to the study of adaptation are often exclusively based on a priori candidate genes or on searching for signals of selection at the DNA level giving us a biased and incomplete picture of the adaptive process.
In this project, we focused on the study of recent transposable element (TE)-induced adaptations in Drosophila melanogaster. Previous results showed that (i) TE-induced adaptations should be common and readily detectable; and (ii) studying different geographical populations should be the most promising approach to identify multiple adaptive insertions. Thus, the first objective of the project was to identify adaptive TE insertions in natural populations from different geographical locations. We chose to analyze two populations located in the extreme of a cline: Sweden and South Italy. We obtained whole genome sequences for 27 strains collected in Sweden and for 16 strains collected in South Italy. The analyses of these 43 genomes, together with the analyses of 141 strains available from a population in North Carolina (USA) and 20 strains available from a population in Rwanda, allowed us to identify 39 putatively adaptive TEs. These 39 TEs are present at low frequencies or absent in Rwanda and at high frequencies in out-of-Africa populations and thus are likely to be involved in adaptation to the out-of-Africa environments. Furthermore, we showed that 15 of the 39 putatively adaptive TEs showed signatures of a selective sweep suggesting that they have increased in frequency due to positive selection.
We further studied the molecular mechanisms and fitness consequences of six putatively adaptive TEs. We found that five of them are involved in stress response: two in cold stress response, one in oxidative stress response, one in heavy-metal stress response, and one in xenobiotic stress response. The other putatively adaptive TE analyzed is associated to faster developmental time. Thus, our results suggest that the ability to cope with stressful environments is an important adaptive trait in natural D. melanogaster populations. Two of these six adaptive TEs affect both the structure and the expression of the nearby gene while another three only affect the expression. In most cases the presence of the adaptive insertion is associated with up-regulation of the nearby gene: four out of five instances. Finally, for two of the characterized adaptive TE insertions, besides finding the adaptive phenotype we were also able to identify the cost of selection of the mutation.
Overall, our results confirmed that TEs are a good tool to study adaptation in natural populations. Moreover, because TEs are present in virtually all organisms that have been studied so far, a role for TEs in adaptive evolution is most probably not restricted to D. melanogaster.