Multigenerational effect of heat stress on the Drosophila melanogaster sperm proteome

Abstract

The notion that genes are the sole units of heredity and that a barrier exists between soma and germline has been a major hurdle in elucidating the heritability of traits that were observed to follow a non-Mendelian inheritance pattern. It was only after the conception of epigenetics by Conrad Waddington that the effect of parental environment on subsequent generations via non-DNA sequence-based mechanisms, such as DNA methylation, chromatin modifications, non-coding RNAs and proteins, could be established, now referred to as multigenerational epigenetic inheritance. Despite growing evidence, the male gamete-derived epigenetic factors that mediate the transmission of such phenotypes are seldom explored, particularly in the model organism Drosophila melanogaster. Using the heat stress-induced multigenerational epigenetic inheritance paradigm in a widely used position-effect variegation line of Drosophila, named white-mottled, we have dissected the effect of heat stress on the sperm proteome in the current study. We demonstrate that multiple successive generations of heat stress at the early embryonic stage results in a significant downregulation of proteins associated with a diverse set of functions, such as translation, chromatin organization, microtubule-based processes, and generation of metabolites and energy, in the sperms. Based on our findings, we propose chromatin-based epigenetic mechanisms, a well-established mechanism for multigenerational effects, as a plausible way of transmitting heat stress memory via the male germline in this case. Moreover, we show that despite these heat stress-induced changes, the life-history traits, such as reproductive fitness and stress tolerance of the subsequent generations, are unaffected, probing the evolutionary relevance of multigenerational epigenetic effects.