Genevieve Housman1,2, Ellen E Quillen3, Anne C Stone1,2. 1. School of Human Evolution and Social Change, Arizona State University, Tempe, Arizona, USA. 2. Center for Evolution and Medicine, Arizona State University, Tempe, Arizona, USA. 3. Department of Genetics, Texas Biomedical Research Institute, San Antonio, Texas, USA.
Abstract
OBJECTIVES: Epigenetic mechanisms influence the development and maintenance of complex phenotypes and may also contribute to the evolution of species-specific phenotypes. With respect to skeletal traits, little is known about the gene regulation underlying these hard tissues or how tissue-specific patterns are associated with bone morphology or vary among species. To begin exploring these topics, this study evaluates one epigenetic mechanism, DNA methylation, in skeletal tissues from five nonhuman primate species which display anatomical and locomotor differences representative of their phylogenetic groups. MATERIALS AND METHODS: First, we test whether intraspecific variation in skeletal DNA methylation is associated with intraspecific variation in femur morphology. Second, we identify interspecific differences in DNA methylation and assess whether these lineage-specific patterns may have contributed to species-specific morphologies. Specifically, we use the Illumina Infinium MethylationEPIC BeadChip to identify DNA methylation patterns in femur trabecular bone from baboons (n = 28), macaques (n = 10), vervets (n = 10), chimpanzees (n = 4), and marmosets (n = 6). RESULTS: Significant differentially methylated positions (DMPs) were associated with a subset of morphological variants, but these likely have small biological effects and may be confounded by other variables associated with morphological variation. Conversely, several species-specific DMPs were identified, and these are found in genes enriched for functions associated with complex skeletal traits. DISCUSSION: Overall, these findings reveal that while intraspecific epigenetic variation is not readily associated with skeletal morphology differences, some interspecific epigenetic differences in skeletal tissues exist and may contribute to evolutionarily distinct phenotypes. This work forms a foundation for future explorations of gene regulation and skeletal trait evolution in primates.
OBJECTIVES: Epigenetic mechanisms influence the development and maintenance of complex phenotypes and may also contribute to the evolution of species-specific phenotypes. With respect to skeletal traits, little is known about the gene regulation underlying these hard tissues or how tissue-specific patterns are associated with bone morphology or vary among species. To begin exploring these topics, this study evaluates one epigenetic mechanism, DNA methylation, in skeletal tissues from five nonhuman primate species which display anatomical and locomotor differences representative of their phylogenetic groups. MATERIALS AND METHODS: First, we test whether intraspecific variation in skeletal DNA methylation is associated with intraspecific variation in femur morphology. Second, we identify interspecific differences in DNA methylation and assess whether these lineage-specific patterns may have contributed to species-specific morphologies. Specifically, we use the Illumina Infinium MethylationEPIC BeadChip to identify DNA methylation patterns in femur trabecular bone from baboons (n = 28), macaques (n = 10), vervets (n = 10), chimpanzees (n = 4), and marmosets (n = 6). RESULTS: Significant differentially methylated positions (DMPs) were associated with a subset of morphological variants, but these likely have small biological effects and may be confounded by other variables associated with morphological variation. Conversely, several species-specific DMPs were identified, and these are found in genes enriched for functions associated with complex skeletal traits. DISCUSSION: Overall, these findings reveal that while intraspecific epigenetic variation is not readily associated with skeletal morphology differences, some interspecific epigenetic differences in skeletal tissues exist and may contribute to evolutionarily distinct phenotypes. This work forms a foundation for future explorations of gene regulation and skeletal trait evolution in primates.
Authors: David Gokhman; Malka Nissim-Rafinia; Lily Agranat-Tamir; Genevieve Housman; Raquel García-Pérez; Esther Lizano; Olivia Cheronet; Swapan Mallick; Maria A Nieves-Colón; Heng Li; Songül Alpaslan-Roodenberg; Mario Novak; Hongcang Gu; Jason M Osinski; Manuel Ferrando-Bernal; Pere Gelabert; Iddi Lipende; Deus Mjungu; Ivanela Kondova; Ronald Bontrop; Ottmar Kullmer; Gerhard Weber; Tal Shahar; Mona Dvir-Ginzberg; Marina Faerman; Ellen E Quillen; Alexander Meissner; Yonatan Lahav; Leonid Kandel; Meir Liebergall; María E Prada; Julio M Vidal; Richard M Gronostajski; Anne C Stone; Benjamin Yakir; Carles Lalueza-Fox; Ron Pinhasi; David Reich; Tomas Marques-Bonet; Eran Meshorer; Liran Carmel Journal: Nat Commun Date: 2020-03-04 Impact factor: 14.919
Authors: Mario Cáceres; Joel Lachuer; Matthew A Zapala; John C Redmond; Lili Kudo; Daniel H Geschwind; David J Lockhart; Todd M Preuss; Carrolee Barlow Journal: Proc Natl Acad Sci U S A Date: 2003-10-13 Impact factor: 11.205
Authors: Bo Zhang; Yan Zhou; Nan Lin; Rebecca F Lowdon; Chibo Hong; Raman P Nagarajan; Jeffrey B Cheng; Daofeng Li; Michael Stevens; Hyung Joo Lee; Xiaoyun Xing; Jia Zhou; Vasavi Sundaram; Ginell Elliott; Junchen Gu; Taoping Shi; Philippe Gascard; Mahvash Sigaroudinia; Thea D Tlsty; Theresa Kadlecek; Arthur Weiss; Henriette O'Geen; Peggy J Farnham; Cécile L Maire; Keith L Ligon; Pamela A F Madden; Angela Tam; Richard Moore; Martin Hirst; Marco A Marra; Baoxue Zhang; Joseph F Costello; Ting Wang Journal: Genome Res Date: 2013-06-26 Impact factor: 9.043
Authors: Mei-Lyn Ong; Peck Yean Tan; Julia L MacIsaac; Sarah M Mah; Jan Paul Buschdorf; Clara Y Cheong; Walter Stunkel; Louiza Chan; Peter D Gluckman; Keefe Chng; Michael S Kobor; Michael J Meaney; Joanna D Holbrook Journal: G3 (Bethesda) Date: 2014-05-08 Impact factor: 3.154
Authors: Elaine E Guevara; William D Hopkins; Patrick R Hof; John J Ely; Brenda J Bradley; Chet C Sherwood Journal: PLoS Genet Date: 2021-05-06 Impact factor: 5.917
Authors: Wanding Zhou; Toshinori Hinoue; Bret Barnes; Owen Mitchell; Waleed Iqbal; Sol Moe Lee; Kelly K Foy; Kwang-Ho Lee; Ethan J Moyer; Alexandra VanderArk; Julie M Koeman; Wubin Ding; Manpreet Kalkat; Nathan J Spix; Bryn Eagleson; John Andrew Pospisilik; Piroska E Szabó; Marisa S Bartolomei; Nicole A Vander Schaaf; Liang Kang; Ashley K Wiseman; Peter A Jones; Connie M Krawczyk; Marie Adams; Rishi Porecha; Brian H Chen; Hui Shen; Peter W Laird Journal: Cell Genom Date: 2022-07-13