Epigenetic programming alterations in alligators from environmentally contaminated lakes

Abstract

Previous studies examining the reproductive health of alligators in Florida lakes indicate that a variety of developmental and health impacts can be attributed to a combination of environmental quality and exposures to environmental contaminants. The majority of these environmental contaminants have been shown to disrupt normal endocrine signaling. The potential that these environmental conditions and contaminants may influence epigenetic status and correlate to the health abnormalities was investigated in the current study. The red blood cell (RBC) (erythrocyte) in the alligator is nucleated so was used as an easily purified marker cell to investigate epigenetic programming. RBCs were collected from adult male alligators captured at three sites in Florida, each characterized by varying degrees of contamination. While Lake Woodruff (WO) has remained relatively pristine, Lake Apopka (AP) and Merritt Island (MI) convey exposures to different suites of contaminants. DNA was isolated and methylated DNA immuno-precipitation (MeDIP) was used to isolate methylated DNA that was then analyzed in a competitive hybridization using a genome-wide alligator tiling array for a MeDIP-Chip analysis. Pairwise comparisons of alligators from AP and MI to WO revealed alterations in the DNA methylome. The AP vs. WO comparison identified 85 differential DNA methylation regions (DMRs) with ⩾3 adjacent oligonucleotide tiling array probes and 15,451 DMRs with a single oligo probe analysis. The MI vs. WO comparison identified 75 DMRs with the ⩾3 oligo probe and 17,411 DMRs with the single oligo probe analysis. There was negligible overlap between the DMRs identified in AP vs. WO and MI vs. WO comparisons. In both comparisons DMRs were primarily associated with CpG deserts which are regions of low CpG density (1–2 CpG/100 bp). Although the alligator genome is not fully annotated, gene associations were identified and correlated to major gene class functional categories and pathways of endocrine relevance. Observations demonstrate that environmental quality may be associated with epigenetic programming and health status in the alligator. The epigenetic alterations may provide biomarkers to assess the environmental exposures and health impacts on these populations of alligators.

Regional epigenetic variation in asexual snail populations among urban and rural lakes

“…However, if epigenetic marks are not stably inherited but instead environmentally sensitive, then any observed epigenetic differences may result from a response to environmental factors, such as the proximity of a site to urbanization and industrialization. For example, environmental toxicants unique to each sample site may explain the presence of epigenetic alterations (as in [11–13]). Lake 2 appears to be the most distinct in terms of methylation alterations.…”

“…Interestingly, sexual species exhibit epigenetic divergence among populations. For example, an examination of three populations of Alligator mississippiens ( American alligator) revealed site-specific epigenetic modifications in two contaminated lakes when compared to a pristine lake [11]. Comparison in differential DNA-methylated regions (DMRs) between each contaminated lake and the pristine lake suggests that epigenetic responses to environmental toxicants and factors can be the result of the specific environment experienced by each population and may be unique between isolated populations.…”

The Model of the Conserved Epigenetic Regulation of Sex

“…These EEMs could therefore be useful in conservation programs aimed at determining the environmental hazards to which natural populations may have been previously exposed. As an example along these lines, Guillette et al (2016) identified epigenetic biomarkers to assess the environmental exposures and health impacts on populations of alligators from lakes contaminated with endocrine-disrupting compounds. The effects of endocrine-disrupting compounds on DNA methylation in the field of aquatic toxicology and biodiversity conservation have recently been reviewed by Tubbs and McDonough, (2018).…”

Synthesizing the role of epigenetics in the response and adaptation of species to climate change in freshwater ecosystems

“…Numerous environmental factors have been shown to influence epigenetic mechanisms (Blake & Watson, 2016;Guillette, Parrott, Nilsson, Haque, & Skinner, 2016;Willbanks et al, 2016). As epigenetic mechanisms can regulate gene expression, the consequence of a given environmental stress scenario can be a change in the phenotype (Burggren, 2016;Manjrekar, 2017;Moore, Le, & Fan, 2013).…”