Early life social and ecological determinants of global DNA methylation in wild spotted hyenas

Zachary M. Laubach; Christopher D. Faulk; Dana C. Dolinoy; Luke Montrose; Tamara R. Jones; Donna Ray; Malit O. Pioon; Kay E. Holekamp

doi:10.1111/mec.15174

Early life social and ecological determinants of global DNA methylation in wild spotted hyenas

Zachary M. Laubach, Christopher D. Faulk, Dana C. Dolinoy, Luke Montrose, Tamara R. Jones, Donna Ray, Malit O. Pioon, Kay E. Holekamp

Animal Science

Research output: Contribution to journal › Article › peer-review

15 Scopus citations

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 3 months 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.

Original language	English (US)
Pages (from-to)	3799-3812
Number of pages	14
Journal	Molecular ecology
Volume	28
Issue number	16
DOIs	https://doi.org/10.1111/mec.15174
State	Published - Aug 1 2019

Bibliographical note

Funding Information:
We thank the Kenyan National Commission for Science, Technology and Innovation, the Kenya Wildlife Service, the Narok County Government, and the Senior Warden of the Masai Mara National Reserve for permission to conduct this research. We are indebted to all those who have contributed to long-term data and sample collection on the Mara Hyena Project. We are also grateful to Dr. Wei Perng for suggestions and feedback regarding the use of life-course epidemiological models. This work was supported by National Science Foundation Grants DEB1353110, OISE1556407 and IOS1755089 to K.E.H., and a Doctoral Dissertation Improvement Grant from NSF (DDIG 1701384) to Z.M.L. This work was also supported in part by funds from NSF Grant OIA 0939454 to the BEACON Center for the Study of Evolution in Action as well as Michigan Lifestage Environmental Exposures and Disease (M-LEEaD), NIEHS Core Center (P30 ES017885), as well as the UM NIEHS Institutional Training Grant T32 ES007062 to D.C.D.

Publisher Copyright:
© 2019 John Wiley & Sons Ltd

Keywords

DNA methylation
Developmental Origins of Health and Disease
mammals
social environment

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10.1111/mec.15174

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title = "Early life social and ecological determinants of global DNA methylation in wild spotted hyenas",

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 3 months 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.",

keywords = "DNA methylation, Developmental Origins of Health and Disease, mammals, social environment",

author = "Laubach, {Zachary M.} and Faulk, {Christopher D.} and Dolinoy, {Dana C.} and Luke Montrose and Jones, {Tamara R.} and Donna Ray and Pioon, {Malit O.} and Holekamp, {Kay E.}",

note = "Funding Information: We thank the Kenyan National Commission for Science, Technology and Innovation, the Kenya Wildlife Service, the Narok County Government, and the Senior Warden of the Masai Mara National Reserve for permission to conduct this research. We are indebted to all those who have contributed to long-term data and sample collection on the Mara Hyena Project. We are also grateful to Dr. Wei Perng for suggestions and feedback regarding the use of life-course epidemiological models. This work was supported by National Science Foundation Grants DEB1353110, OISE1556407 and IOS1755089 to K.E.H., and a Doctoral Dissertation Improvement Grant from NSF (DDIG 1701384) to Z.M.L. This work was also supported in part by funds from NSF Grant OIA 0939454 to the BEACON Center for the Study of Evolution in Action as well as Michigan Lifestage Environmental Exposures and Disease (M-LEEaD), NIEHS Core Center (P30 ES017885), as well as the UM NIEHS Institutional Training Grant T32 ES007062 to D.C.D. Publisher Copyright: {\textcopyright} 2019 John Wiley & Sons Ltd",

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language = "English (US)",

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AU - Faulk, Christopher D.

AU - Dolinoy, Dana C.

AU - Montrose, Luke

AU - Jones, Tamara R.

AU - Ray, Donna

AU - Pioon, Malit O.

AU - Holekamp, Kay E.

N1 - Funding Information: We thank the Kenyan National Commission for Science, Technology and Innovation, the Kenya Wildlife Service, the Narok County Government, and the Senior Warden of the Masai Mara National Reserve for permission to conduct this research. We are indebted to all those who have contributed to long-term data and sample collection on the Mara Hyena Project. We are also grateful to Dr. Wei Perng for suggestions and feedback regarding the use of life-course epidemiological models. This work was supported by National Science Foundation Grants DEB1353110, OISE1556407 and IOS1755089 to K.E.H., and a Doctoral Dissertation Improvement Grant from NSF (DDIG 1701384) to Z.M.L. This work was also supported in part by funds from NSF Grant OIA 0939454 to the BEACON Center for the Study of Evolution in Action as well as Michigan Lifestage Environmental Exposures and Disease (M-LEEaD), NIEHS Core Center (P30 ES017885), as well as the UM NIEHS Institutional Training Grant T32 ES007062 to D.C.D. Publisher Copyright: © 2019 John Wiley & Sons Ltd

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N2 - 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 3 months 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.

AB - 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 3 months 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.

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KW - Developmental Origins of Health and Disease

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Early life social and ecological determinants of global DNA methylation in wild spotted hyenas

Abstract

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