Abstract

Environmental factors early in life can have lasting influence on the development and phenotypes of animals, but the underlying molecular modifications remain poorly understood. We examined cross-sectional associations among early life socioecological factors and global DNA methylation in 293 wild spotted hyenas (Crocuta crocuta) in the Masai Mara National Reserve, Kenya, grouped according to three age classes (cub, subadult and adult). Explanatory variables of interest included annual maternal rank based on outcomes of dyadic agonistic interactions, litter size, wild ungulate prey density and anthropogenic disturbance in the year each hyena was born based on counts of illegal livestock in the Reserve. The dependent variable of interest was global DNA methylation, assessed via the LUminometric Methylation Assay, which provides a percentage methylation value calculated at CCGG sites across the genome. Among cubs, we observed approximately 2.75% higher CCGG methylation in offspring born to high- than low-ranking mothers. Among cubs and subadults, higher anthropogenic disturbance corresponded with greater %CCGG methylation. In both cubs and adults, we found an inverse association between prey density measured before a hyena was 3months old and %CCGG methylation. Our results suggest that maternal rank, anthropogenic disturbance and prey availability early in life are associated with later life global DNA methylation. Future studies are required to understand the extent to which these DNA methylation patterns relate to adult phenotypes and fitness outcomes.

Highlights

  • The Developmental Origins of Health and Disease (DOHaD) hypothesis suggests that environmental conditions over the course of ontogeny have lasting effects on an organism’s phenotype (Gillman, 2005)

  • We found that, compared to cubs born into low anthropogenic disturbance, cubs from medium anthropogenic disturbance groups had 2.88 (95%CI: 0.99, 4.78; P = 0.004) %CCGG higher methylation and cubs born into high disturbance had 3.51 (95%CI: 0.83, 6.19; P = 0.013) %CCGG higher methylation

  • In line with our expectations, we found that higher maternal rank at birth was associated with higher global DNA methylation in offspring sampled as cubs, but not in those sampled as subadults or adults

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Summary

Introduction

The Developmental Origins of Health and Disease (DOHaD) hypothesis suggests that environmental conditions over the course of ontogeny have lasting effects on an organism’s phenotype (Gillman, 2005). Of particular interest in DOHaD are vulnerable developmental stages (“sensitive periods”) marked by high phenotypic plasticity (Heindel & Vandenberg, 2015). Such as the periconceptional period, gestation, and the early post-natal period (Gluckman, Cutfield, Hofman, & Hanson, 2005; Hanson & Gluckman, 2014). DNA methylation as a pathway of DOHaD phenomena. One molecular pathway hypothesized to underlie DOHaD phenomena involves DNA methylation (Waterland & Michels, 2007). Of particular relevance to DOHaD is the fact that DNA methylation is a well-characterized and mitotically stable epigenetic modification that is both responsive to environmental factors, and associated with gene regulation and phenotype When considering the potential biological impact of DNA methylation, a key consideration is that its biological function (e.g. permissive vs. repressive effects on gene expression) depend in large part on where DNA methylation occurs within the genome – i.e., in repetitive elements, gene promoter regions, or gene bodies (Jones, 2012; Schübeler, 2015)

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