Genetic characterization of a captive marmoset (Callithrix jacchus) colony using genotype-by-sequencing.

Callithrix jacchus biomedical research captive nonhuman primates genetic ancestry hair follicle DNA pedigree

Journal

American journal of primatology
ISSN: 1098-2345
Titre abrégé: Am J Primatol
Pays: United States
ID NLM: 8108949

Informations de publication

Date de publication:
24 Apr 2024
Historique:
revised: 27 03 2024
received: 27 06 2023
accepted: 14 04 2024
medline: 24 4 2024
pubmed: 24 4 2024
entrez: 24 4 2024
Statut: aheadofprint

Résumé

The marmoset is a fundamental nonhuman primate model for the study of aging, neurobiology, and many other topics. Genetic management of captive marmoset colonies is complicated by frequent chimerism in the blood and other tissues, a lack of tools to enable cost-effective, genome-wide interrogation of variation, and historic mergers and migrations of animals between colonies. We implemented genotype-by-sequencing (GBS) of hair follicle derived DNA (a minimally chimeric DNA source) of 82 marmosets housed at the Southwest National Primate Research Center (SNPRC). Our primary goals were the genetic characterization of our marmoset population for pedigree verification and colony management and to inform the scientific community of the functional genetic makeup of this valuable resource. We used the GBS data to reconstruct the genetic legacy of recent mergers between colonies, to identify genetically related animals whose relationships were previously unknown due to incomplete pedigree information, and to show that animals in the SNPRC colony appear to exhibit low levels of inbreeding. Of the >99,000 single-nucleotide variants (SNVs) that we characterized, >9800 are located within gene regions known to harbor pathogenic variants of clinical significance in humans. Overall, we show the combination of low-resolution (sparse) genotyping using hair follicle DNA is a powerful strategy for the genetic management of captive marmoset colonies and for identifying potential SNVs for the development of biomedical research models.

Identifiants

pubmed: 38655843
doi: 10.1002/ajp.23630
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e23630

Subventions

Organisme : NIH HHS
ID : P51 RR013986
Pays : United States

Informations de copyright

© 2024 Wiley Periodicals LLC.

Références

Abbott, D. H., Barnett, D. K., Colman, R. J., Yamamoto, M. E., & Schultz‐Darken, N. J. (2003). Aspects of common marmoset basic biology and life history important for biomedical research. Comparative Medicine, 53(4), 339–350.
Alexander, D. H., Shringarpure, S. S., Novembre, J., & Lange, K. (2015). Admixture 1.3 software manual. UCLA Human Genetics Software Distribution.
Almasy, L., & Blangero, J. (1998). Multipoint quantitative‐trait linkage analysis in general pedigrees. The American Journal of Human Genetics, 62(5), 1198–1211.
Van der Auwera, G. A. & O'Connor, B. D. (2020). Genomics in the cloud: using Docker, GATK, and WDL in Terra. O'Reilly Media.
Benirschke, K., Anderson, J. M., & Brownhill, L. E. (1962). Marrow chimerism in marmosets. Science, 138(3539), 513–515.
Bimber, B. N., Raboin, M. J., Letaw, J., Nevonen, K. A., Spindel, J. E., McCouch, S. R., Cervera‐Juanes, R., Spindel, E., Carbone, L., Ferguson, B., & Vinson, A. (2016). Whole‐genome characterization in pedigreed non‐human primates using genotyping‐by‐sequencing (GBS) and imputation. BMC Genomics, 17(1), 676.
Chan, J., Yao, W., Howard, T. D., Hawkins, G. A., Olivier, M., Jorgensen, M. J., Cheeseman, I. H., Cole, S. A., & Cox, L. A. (2021). Efficiency of whole‐exome sequencing in old world and new world primates using human capture reagents. Journal of Medical Primatology, 50(3), 176–181.
Cheng, J. Y., Stern, A. J., Racimo, F., & Nielsen, R. (2022). Detecting selection in multiple populations by modeling ancestral admixture components. Molecular Biology and Evolution, 39(1), msab294.
Cline, M. S., & Karchin, R. (2011). Using bioinformatics to predict the functional impact of SNVs. Bioinformatics, 27(4), 441–448.
Dixson, A. F., Hastie, N., Patel, I., & Jeffreys, A. J. (1988). DNA ‘fingerprinting’ of captive family groups of common marmosets (Callithrix jacchus). Folia Primatologica, 51(1), 52–55.
Dyke, B. (1996). PEDSYS: A pedigree data management system. Population Genetics. Laboratory, Department of Genetics, Southwest Foundation for Biomedical Research, San Antonio.
Elshire, R. J., Glaubitz, J. C., Sun, Q., Poland, J. A., Kawamoto, K., Buckler, E. S., & Mitchell, S. E. (2011). A robust, simple genotyping‐by‐sequencing (GBS) approach for high diversity species. PLoS One, 6(5), e19379.
Faulkes, C. G., Arruda, M. F., & Monteiro da Cruz, M. A. O. (2003). Matrilineal genetic structure within and among populations of the cooperatively breeding common marmoset, Callithrix jacchus. Molecular Ecology, 12(4), 1101–1108.
Forman, L., Kleiman, D. G., Bush, R. M., Dietz, J. M., Ballou, J. D., Phillips, L. G., Coimbra‐Filho, A. F., & O'Brien, S. J. (1986). Genetic variation within and among lion tamarins. American Journal of Physical Anthropology, 71(1), 1–11.
Harding, J. D. (2017). Nonhuman primates and translational research: progress, opportunities, and challenges. ILAR Journal, 58(2), 141–150.
Harris, R. A., Raveendran, M., Warren, W., LaDeana, H. W., Tomlinson, C., Graves‐Lindsay, T., Green, R. E., Schmidt, J. K., Colwell, J. C., Makulec, A. T., Cole, S. A., Cheeseman, I. H., Ross, C. N., Capuano, S., Eichler, E. E., Levine, J. E., & Rogers, J. (2023). Whole genome analysis of SNV and indel polymorphism in common marmosets (Callithrix jacchus). Genes, 14(12), 2185.
Haus, T., Ferguson, B., Rogers, J., Doxiadis, G., Certa, U., Rose, N. J., Teepe, R., Weinbauer, G. F., & Roos, C. (2014). Genome typing of nonhuman primate models: implications for biomedical research. Trends in Genetics, 30(11), 482–487.
Herten, K., Hestand, M. S., Vermeesch, J. R., & Van Houdt, J. K. (2015). GBSX: a toolkit for experimental design and demultiplexing genotyping by sequencing experiments. BMC Bioinformatics, 16(1), 73.
Honess, P., Stanley‐Griffiths, M. A., Narainapoulle, S., Naiken, S., & Andrianjazalahatra, T. (2010). Selective breeding of primates for use in research: consequences and challenges. Animal Welfare, 19(S1), 57–65.
Huang, Y. S., Ramensky, V., Service, S. K., Jasinska, A. J., Jung, Y., Choi, O. W., Cantor, R. M., Juretic, N., Wasserscheid, J., Kaplan, J. R., Jorgensen, M. J., Dyer, T. D., Dewar, K., Blangero, J., Wilson, R. K., Warren, W., Weinstock, G. M., & Freimer, N. B. (2015). Sequencing strategies and characterization of 721 vervet monkey genomes for future genetic analyses of medically relevant traits. BMC Biology, 13(1), 1–10.
Jasinska, A. J. (2020). Resources for functional genomic studies of health and development in nonhuman primates. American Journal of Physical Anthropology, 171, 174–194.
Kishi, N., Sato, K., Sasaki, E., & Okano, H. (2014). Common marmoset as a new model animal for neuroscience research and genome editing technology. Development, Growth & Differentiation, 56(1), 53–62.
Li, H. (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA‐MEM. arXiv preprint arXiv:1303.3997, 1303.3997.
Lipatov, M., Sanjeev, K., Patro, R., & Veeramah, K. R. (2015). Maximum likelihood estimation of biological relatedness from low coverage sequencing data. BioRxiv, 023374.
Marini, R. P., Wachtman, L. M., Tardif, S. D., Mansfield, K., & Fox, J. G. (2018). The common marmoset in captivity and biomedical research. Academic Press.
McLaren, W., Gil, L., Hunt, S. E., Riat, H. S., Ritchie, G. R. S., Thormann, A., Flicek, P., & Cunningham, F. (2016). The ensembl variant effect predictor. Genome Biology, 17(1), 122.
MGSAC. (2014). The common marmoset genome provides insight into primate biology and evolution. Nature Genetics, 46, 850–857. https://doi.org/10.1038/ng.3042
Miller, C. T. (2017). Why marmosets? Developmental Neurobiology, 77, 237–243.
Miller, C. T., Freiwald, W. A., Leopold, D. A., Mitchell, J. F., Silva, A. C., & Wang, X. (2016). Marmosets: A neuroscientific model of human social behavior. Neuron, 90(2), 219–233.
Moshiri, A., Chen, R., Kim, S., Harris, R. A., Li, Y., Raveendran, M., Davis, S., Liang, Q., Pomerantz, O., Wang, J., Garzel, L., Cameron, A., Yiu, G., Stout, J. T., Huang, Y., Murphy, C. J., Roberts, J., Gopalakrishna, K. N., Boyd, K., … Thomasy, S. M. (2019). A nonhuman primate model of inherited retinal disease. Journal of Clinical Investigation, 129(2), 863–874.
National Academies of Sciences, E., & Medicine. (2019). Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing‐Based Biomedical Research: Proceedings of a Workshop.
Nievergelt, C. M., Digby, L. J., Ramakrishnan, U., & Woodruff, D. S. (2000). Genetic analysis of group composition and breeding system in a wild common marmoset (Callithrix jacchus) population. International Journal of Primatology, 21, 1–20.
Rogers, J., & del Rosario, R. (2019). Marmoset Genomics and Genetic Diversity. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing‐Based Biomedical Research: Proceedings of a Workshop.
Ross, C. N., French, J. A., & Ortí, G. (2007). Germ‐line chimerism and paternal care in marmosets (Callithrix kuhlii). Proceedings of the National Academy of Sciences, 104(15), 6278–6282.
Ross, C. N. & Salmon, A. B. (2019). Aging research using the common marmoset: Focus on aging interventions. Nutrition and healthy aging, 5(2), 97–109.
Sato, K., Kuroki, Y., Kumita, W., Fujiyama, A., Toyoda, A., Kawai, J., Iriki, A., Sasaki, E., Okano, H., & Sakakibara, Y. (2015). Resequencing of the common marmoset genome improves genome assemblies and gene‐coding sequence analysis. Scientific Reports, 5(1), 16894.
Schoener, T. W. (2011). The newest synthesis: understanding the interplay of evolutionary and ecological dynamics. Science, 331(6016), 426–429.
Servick, K. (2018). US labs clamor for marmosets. In: American Association for the Advancement of Science.
Shriner, D. (2017). Overview of admixture mapping. Current protocols in human genetics, 94(1), 1.23. 21–21.23. 28.
Silva, M. O. M., Armada, J. L. A. D., Verona, C. E. S., Heliodoro, G., & Nogueira, D. M. (2017). Cytogenetics and molecular genetic analysis of chimerism in marmosets (Callithrix: Primates). Anais da Academia Brasileira de Ciências, 89, 2793–2804.
Sinnwell, J. P., Therneau, T. M., & Schaid, D. J. (2014). The kinship2 R package for pedigree data. Human Heredity, 78(2), 91–93.
Sobel, E., Sengul, H., & Weeks, D. E. (2001). Multipoint estimation of identity‐by‐descent probabilities at arbitrary positions among marker loci on general pedigrees. Human Heredity, 52(3), 121–131.
Sweeney, C. G., Curran, E., Westmoreland, S. V., Mansfield, K. G., & Vallender, E. J. (2012). Quantitative molecular assessment of chimerism across tissues in marmosets and tamarins. BMC Genomics, 13(1), 98.
Takabayashi, S. & Katoh, H. (2015). Noninvasive genotyping of common marmoset (Callithrix jacchus) by fingernail PCR. Primates, 56(3), 235–240.
Tardif, S. D., & Ross, C. N. (2019). Reproduction, Growth, and Development, The Common Marmoset in Captivity and Biomedical Research (pp. 119–132). Elsevier.
Tardif, S. D., Smucny, D. A., Abbott, D. H., Mansfield, K., Schultz‐Darken, N., & Yamamoto, M. E. (2003). Reproduction in captive common marmosets (Callithrix jacchus). Comparative Medicine, 53(4), 364–368.
Watkins, D., Garber, T., Chen, Z., Toukatly, G., Hughes, A., & Letvin, N. (1991). Unusually limited nucleotide sequence variation of the expressed major histocompatibility complex class I genes of a new world primate species (Saguinus oedipus). Immunogenetics, 33, 79–89.
Xue, C., Raveendran, M., Harris, R. A., Fawcett, G. L., Liu, X., White, S., Dahdouli, M., Rio Deiros, D., Below, J. E., Salerno, W., Cox, L., Fan, G., Ferguson, B., Horvath, J., Johnson, Z., Kanthaswamy, S., Kubisch, H. M., Liu, D., Platt, M., … Rogers, J. (2016). The population genomics of rhesus macaques (Macaca mulatta) based on whole‐genome sequences. Genome Research, 26(12), 1651–1662.

Auteurs

Shelley A Cole (SA)

Southwest National Primate Research Center, San Antonio, Texas, USA.
Texas Biomedical Research Institute, San Antonio, Texas, USA.

Martha M Lyke (MM)

Southwest National Primate Research Center, San Antonio, Texas, USA.
Texas Biomedical Research Institute, San Antonio, Texas, USA.

Clinton Christensen (C)

Southwest National Primate Research Center, San Antonio, Texas, USA.
Texas Biomedical Research Institute, San Antonio, Texas, USA.

Deborah Newman (D)

Southwest National Primate Research Center, San Antonio, Texas, USA.
Texas Biomedical Research Institute, San Antonio, Texas, USA.

Alec Bagwell (A)

Southwest National Primate Research Center, San Antonio, Texas, USA.
Texas Biomedical Research Institute, San Antonio, Texas, USA.

Samuel Galindo (S)

Southwest National Primate Research Center, San Antonio, Texas, USA.
Texas Biomedical Research Institute, San Antonio, Texas, USA.

Jeremy Glenn (J)

Texas Biomedical Research Institute, San Antonio, Texas, USA.

Donna G Layne-Colon (DG)

Southwest National Primate Research Center, San Antonio, Texas, USA.
Texas Biomedical Research Institute, San Antonio, Texas, USA.

Ken Sayers (K)

Southwest National Primate Research Center, San Antonio, Texas, USA.
Texas Biomedical Research Institute, San Antonio, Texas, USA.

Suzette Tardif (S)

Southwest National Primate Research Center, San Antonio, Texas, USA.

Laura A Cox (LA)

Center for Precision Medicine, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA.

Corinna Ross (C)

Southwest National Primate Research Center, San Antonio, Texas, USA.
Texas Biomedical Research Institute, San Antonio, Texas, USA.

Ian H Cheeseman (IH)

Southwest National Primate Research Center, San Antonio, Texas, USA.
Texas Biomedical Research Institute, San Antonio, Texas, USA.

Classifications MeSH