Stress, transposons and genome evolution

After Darwin's book on the origin of species by the natural selection, the theory of his precursor Lamarck was never completely abandoned. Over time, the observation of strange natural phenomena has occasionally resurrected the concept of the heredity of acquired characters. To explain, in Darwinian sense, some of the apparent Lamarckian-like phenomena, Waddington elaborated the “canalization and assimilation” concepts (Waddington, 1959). He observed that some phenotypic traits induced in Drosophila pupae by heat shock treatment and selected for a number of generations in the presence of the same stress, became heritable, thereby showing that an induced phenotypic trait could be inherited trough the germ line. Waddington hypothesized the existence of a cryptic genetic variation that is maintained hidden due to the robustness of the developmental process that he indicated as “canalization”. If an environmental stress is strong enough to overcome this robustness, the development pathway can change because of the expression of a cryptic genetic variant. Then, this variant can be selected and become heritable by an “assimilation” process. During the last few years, data supporting this view and providing possible molecular explanations were published. Rutheford and Lindquist (1998) showed that, in Drosophila, impairment of Hsp90 function induces morphogenetic variants that occasionally became fixed and stably transmitted. The interpretation was that Hsp90 is a capacitor of morphological evolution and buffers a pre-existing genetic variation that is not expressed and accumulates in neutral conditions. The stress sensitive storage and release of genetic variation by Hsp90 would favour adaptive evolution. However, our recent study has suggested a different explanation of these results (Specchia et al., 2010). It has been demonstrated that Hsp90 is involved in repression of transcription and mobilization of transposable elements in germ cells by affecting piRNA biogenesis. The reduction of HSP90 causes stress response-like activation and transposition of mobile elements along with a wide range of phenotypic variants due to the transposon insertions to the corresponding genes. On the basis of these observations, we have suggested that Hsp90, rather than functioning as a capacitor, acts, when absent, as a mutator, capable of causing activation and transposition of mobile elements through impairment of piRNAi silencing. Consequently, we propose that stress causes the activation of transposons that would induce de novo gene mutations, affecting development pathways; mutations can be expressed and fixed across subsequent generations by an assimilation process consisting of a co-selection of a somatic and a germinal event giving the same phenotype. This view implies that transposon activation is a major reaction of genomes to environmental stresses and represents a powerful adaptive response.