Abstract
Epigenetic mechanisms convey environmental information through generations and can regulate gene expression. Epigenetic studies in wild mammals are rare, but enable understanding adaptation processes as they may occur in nature. In most wild mammal species, males are the dispersing sex and thus often have to cope with differing habitats and thermal changes more rapidly than the often philopatric females. As temperature is a major environmental selection factor, we investigated whether genetically heterogeneous Wild guinea pig (Cavia aperea) males adapt epigenetically to an increase in temperature, whether that response will be transmitted to the next generation(s), and whether it regulates mRNA expression. Five (F0) adult male guinea pigs were exposed to an increased ambient temperature for 2 months, corresponding to the duration of the species' spermatogenesis. To study the effect of heat, we focused on the main thermoregulatory organ, the liver. We analyzed CpG‐methylation changes of male offspring (F1) sired before and after the fathers' heat treatment (as has recently been described in Weyrich et al. [Mol. Ecol., 2015]). Transcription analysis was performed for the three genes with the highest number of differentially methylated changes detected: the thermoregulation gene Signal Transducer and Activator of Transcription 3 (Stat3), the proteolytic peptidase gene Cathepsin Z (Ctsz), and Sirtuin 6 (Sirt6) with function in epigenetic regulation. Stat3 gene expression was significantly reduced (P < 0.05), which indicated a close link between CpG‐methylation and expression levels for this gene. The two other genes did not show gene expression changes. Our results indicate the presence of a paternal transgenerational epigenetic effect. Quick adaptation to climatic changes may become increasingly relevant for the survival of wildlife species as global temperatures are rising.
Highlights
Past epigenetic studies have mainly focused on medical and developmental aspects in humans and model species, while studies on ecologically relevant traits in nonmodel species are still scarce (Richards 2006; Pertoldi and Bach 2007; Bossdorf et al 2008)
We focussed on the three genes with the greatest abundance of significant mCpG-differences between control and heat group: the thermoregulatory gene, Signal Transducer and Activator of Transcription 3 (Stat3); the Cathepsin Z gene (Ctsz), a lysosomal cysteine proteinase with function in tumorigenesis; and the Sirtuin 6 gene (Sirt6), a gene with function in intercellular and epigenetic regulation (Fig. 1)
Our results demonstrate a paternal effect on DNA methylation patterns of the generation after exposure to a 2016 The Authors
Summary
Past epigenetic studies have mainly focused on medical and developmental aspects in humans and model species, while studies on ecologically relevant traits in nonmodel species are still scarce (Richards 2006; Pertoldi and Bach 2007; Bossdorf et al 2008). The regulation of gene expression is fundamental for immediate adaptation processes in the same generation. The inheritance of responses to experienced changes (adapted traits) is fundamental for long-term adaptational memory and evolutionary processes. The mechanism regulating gene expression and conferring such immediate and inherited adaptation is “epigenetic response” (Jablonka and Raz 2009). This response is achieved by epigenetic marks, including DNA methylation, histone modifications, polycomb proteins, and siRNAs, which are controlling the accessibility of the chromatin to the transcriptional machinery. The best-studied epigenetic modification is DNA methylation (e.g., Boyes and Bird 1991; Tate and Bird 1993; Jones and Takai 2001; Bird 2002)
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