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Mol Biol Evol. 2019 Mar 1;36(3):527-540. doi: 10.1093/molbev/msy227.

Evolution of DNA Methylation in Papio Baboons.

Vilgalys TP1, Rogers J2,3, Jolly CJ4,5,6, Mukherjee S7,8,9, Tung J1,10,11,12.

Author information

1
Department of Evolutionary Anthropology, Duke University, Durham, NC.
2
Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX.
3
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX.
4
Department of Anthropology, New York University, New York, NY.
5
Center for the Study of Human Origins, New York University, New York, NY.
6
New York Consortium for Evolutionary Primatology, New York, NY.
7
Department of Statistical Science, Duke University, Durham, NC.
8
Department of Mathematics, Duke University, Durham, NC.
9
Department of Computer Science, Duke University, Durham, NC.
10
Department of Biology, Duke University, Durham, NC.
11
Duke University Population Research Institute, Duke University, Durham, NC.
12
Institute of Primate Research, National Museums of Kenya, Karen, Nairobi, Kenya.

Abstract

Changes in gene regulation have long been thought to play an important role in primate evolution. However, although a number of studies have compared genome-wide gene expression patterns across primate species, fewer have investigated the gene regulatory mechanisms that underlie such patterns, or the relative contribution of drift versus selection. Here, we profiled genome-scale DNA methylation levels in blood samples from five of the six extant species of the baboon genus Papio (4-14 individuals per species). This radiation presents the opportunity to investigate DNA methylation divergence at both shallow and deeper timescales (0.380-1.4 My). In contrast to studies in human populations, but similar to studies in great apes, DNA methylation profiles clearly mirror genetic and geographic structure. Divergence in DNA methylation proceeds fastest in unannotated regions of the genome and slowest in regions of the genome that are likely more constrained at the sequence level (e.g., gene exons). Both heuristic approaches and Ornstein-Uhlenbeck models suggest that DNA methylation levels at a small set of sites have been affected by positive selection, and that this class is enriched in functionally relevant contexts, including promoters, enhancers, and CpG islands. Our results thus indicate that the rate and distribution of DNA methylation changes across the genome largely mirror genetic structure. However, at some CpG sites, DNA methylation levels themselves may have been a target of positive selection, pointing to loci that could be important in connecting sequence variation to fitness-related traits.

KEYWORDS:

DNA methylation; baboons; gene regulation; genetic divergence; molecular evolution; neutral evolution

PMID:
30521003
PMCID:
PMC6389319
[Available on 2020-03-01]
DOI:
10.1093/molbev/msy227
[Indexed for MEDLINE]

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