Phenotypic plasticity, chromatin regulation and evolvability

In developmental studies performed in laboratory conditions, environmental parameters are usually fixed in order to focus on genetic factors. However, gene X environment interactions play a major role in the wild where species live and evolve in spatially and temporally heterogeneous environments. Some species are able to interpret environmental clues to produce different phenotypes, optimal in each environment (adaptive phenotypic plasticity) (Via et al., 1995). A famous example is the seasonal variation in coat color of the snow hare, which allows an optimal camouflage in both summer and winter. In other cases, the influence of the environment is rather deleterious and different mechanisms are used to limit it. Environmental canalization allows a given genotype to produce a stable phenotype despite environmental changes. Chromatin regulators, molecular chaperones such as Hsp90 or redundant regulatory sequences (shadow enhancers) contribute to the canalization of particular traits (Frankel et al., 2010; Sangster et al., 2008; Sollars et al., 2003). Genetic compensation allows distinct genotypes living in different environments to produce the same optimal phenotype because they compensate for the effect of the environment (Grether, 2005). For example, fish populations adjust the efficiency of carotenoid pigments assimilation to the level of carotenoid available in their diet (Grether, 2005). The role of Gene X environment interactions in evolution has been actively discussed as new phenotypic variation can be revealed by environmental changes and assimilated later during evolution (Grether, 2005; Moczek, 2007; Price et al., 2003; Waddington, 1959; West-Eberhard, 2005). Artificial selection experiments have indeed shown that it is possible to dramatically alter the reaction norms of plastic traits (Scharloo, 1962; Suzuki and Nijhout, 2006; Waddington, 1959).

The fruitfly Drosophila melanogaster is an ideal model to study gene X environment interactions because it is both one of the best genetic model and a cosmopolitan species locally adapted to a wide range of environmental conditions. Latitudinal clinal variation is observed for many environment sensitive traits, which shows that it is adaptive (Gibert et al., 2004). Interestingly, particular traits showing thermal plasticity and polymorphism in D. melanogaster (abdominal or thoracic pigmentation patterns) are absent or fixed in other species of Drosophila.


Furthermore, mutations in several regulatory genes, at particular temperature, phenocopy traits observed in other species but normally absent in D. melanogaster (distal sex comb) (Gibert et al., 2007).

It makes these traits interesting models to study how gene X environment interactions influence morphological evolution, although other temperature sensitive traits (male fertility or ovary development) might be the major correlated traits under local selection.

We have linked the thermal plasticity of some of these traits to temperature sensitive chromatin regulation of particular developmental regulatory genes such as cubitus interruptus (ci), encoding the effector of the Hedgehog signaling pathway.

Interestingly, in particular species of Drosophila, ci is located in a different chromatin environment (Larsson et al., 2001; Podemski et al., 2001), which might have strongly conditioned the plasticity and the evolution of particular traits in these species.

Functional natural variation or evidence of positive selection have been identified in several genes acting upstream or downstream of ci in Drosophila melanogaster (Beisswanger and Stephan, 2008; Harr et al., 2002; Kopp et al., 2003; Mezey et al., 2005; Rebeiz et al., 2009; Takahashi et al., 2007). This suggests that many components of these temperature sensitive regulatory networks respond locally to selection. Our analysis started by the study of the variation and the roles of the chromatin regulator Cramped. Our goal is to extend these observations to the whole genome and to dissect these temperature sensitive gene regulatory networks in D. melanogaster at the biochemical, transcriptional and epigenetic level (histone marks; DNA methylation). We will analyze how these networks behave in relation to the traits they control, in different temperature conditions and in different genetic backgrounds (different geographical origin, lines selected artificially for divergent phenotypes, translocations modifying distance of particular genes to constitutive heterochromatin, regulatory gene mutants). We think that by analyzing how environmental conditions, developmental and genomic constraints integrate to produce the phenotype it might be possible to explain differences of evolvability among traits.

References:

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