Phenotypic and epigenetic variation in D. melanogaster and in A. pisum.

(A) Drosophila life cycle and distribution of frequency- and density-dependent foraging (for) alleles depending on rearing conditions. Dark triangles: for^R alleles. Red triangles: for^S alleles. At high density (A and middle alignment of boxes) the for^R allele predominates, whereas at low density (B and bottom alignment) the for^S allele does. (B) An aphid ovariole stained in green for anti HRP (antibody which regognizes an epitope on the membrane). (C) Phenotypic variation of colors obtained from a single aphid mother founder. At 8°C, aphids change from orange to green. (D) Methyl-collected fragment analyzed by bisulfite sequencing to obtain the statistical analysis of methyl cytosine on multiple sites.

Research topics

A striking feature of insects is their ability to adapt rapidly to environmental changes, even for species as aphids that mostly reproduce clonally, reducing genetic variability. Aphids show indeed a high level of phenotypic plasticity, as illustrated by their aptitude to shift their reproduction mode depending on seasons, plant hosts and abiotic factors such as the temperature. However, mechanisms underlying this behavioral plasticity remain largely unknown.

Up to now, the dogma postulates that evolution and genome plasticity are written in the genetic code. In contrast, many recent reports describe that identical genomes might lead to different heritable characters depending on environmental factors. This leads to the new paradigm that environment induces heritable variants that might vanish with time when the conditions having induced them have disappeared. By which mechanisms a gene can be made durably active or inactive through generations when the genome sequences are identical? Recent advances to this question constitute the new active field of epigenetics.

Epigenetic marks are chemical modifications of DNA and histones that occur in all living organisms, mainly through methylation. We are interested in investigating the potential of stable epigenetic marks that might contribute to lasting and heritable phenotypes in insects. Although efficient transgenesis techniques do not yet exist for aphids as they do for Drosophila, the aphid Acyrthosiphon pisum model used in this proposal has a major advantage for epigenetic studies: aphids undergo parthenogenetic reproduction in spring and summer and sexual reproduction in fall, leading to fertilized eggs entering diapause during winter. We found that clonality in A. pisum generates a repertoire of phenotypic variants presenting a high degree of molecular polymorphism that seems stochastically produced and from which individual profiles are environmentally selected. We demonstrated that aphid variants in clonality context are correlated with methylation of the aphid genome and methylation of endosymbionts (unpublished data).

Objectives

One objective of the team is to use the aphid model to determine the components of epigenetic regulation leading to adaptation to the environment. Our aim is to determine whether epigenetic marks, in particular genome methylation, induced by an extreme climate phase might be heritable across clonality (spring and summer) and also whether this heritability might pass the sexual barrier (fall and winter) to be transmitted in the newly emerged clonal generations the next spring, in order to achieve adaptation.

Although fascinating and important, the aphid model has limited genetic tools to decipher the mechanisms of epigenetic variation. Thus, we aim to couple aphid biology to Drosophila genetics in order to elucidate the underlying mechanisms at stake in insects. We plan, as a first step, to develop in Drosophila a genetic mutant-based approach to determine the role of known genes involved in DNA methylation on the regulation of “frequency- and density-dependent genes”. Another strategy will be to identify Drosophila homologous genes of aphid genes involved in epigenetic variations to unravel the underlying molecular mechanisms. The integration of these two models might highlight the molecular pathways leading to adaptation to fluctuating environments and the heredity of epigenetic marks in insects.