Abstract
Owl monkeys (genus Aotus) constitute a remarkable radiation of platyrrhine primates that exhibit many lineage-specific adaptations and evolutionary innovations. Understanding the biology and evolution of owl monkeys requires detailed investigation of both the environmental context of their evolution and the molecular genetics and developmental bases of their unique phenotypes. Analysis of Aotus genetics and genomics will play a critical role in future studies of these animals. Recently, we and our colleagues developed a whole genome reference assembly for Aotus nancymaae (Anan_2.0), the first publicly available reference genome for any Aotus species. This reference assembly constitutes a valuable research resource for a wide range of future studies concerning the biology and evolution of this species and others in the genus. This chapter summarizes initial analyses of this reference genome and suggests further studies that will extend our knowledge of Aotus biology through molecular genetic studies, which were not previously feasible.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Bakken TE, Miller JA, Ding SL, Sunkin SM, Smith KA, Ng L et al (2016) A comprehensive transcriptional map of primate brain development. Nature 535(7612):367–375. https://doi.org/10.1038/nature18637
Bergstrom A, McCarthy SA, Hui R, Almarri MA, Ayub Q, Danecek P et al (2020) Insights into human genetic variation and population history from 929 diverse genomes. Science 367(6484). https://doi.org/10.1126/science.aay5012
Braso-Vives M, Povolotskaya IS, Hartasanchez DA, Farre X, Fernandez-Callejo M, Raveendran M et al (2020) Copy number variants and fixed duplications among 198 rhesus macaques (Macaca mulatta). PLoS Genet 16(5):e1008742. https://doi.org/10.1371/journal.pgen.1008742
Castelijns B, Baak ML, Timpanaro IS, Wiggers CRM, Vermunt MW, Shang P et al (2020) Hominin-specific regulatory elements selectively emerged in oligodendrocytes and are disrupted in autism patients. Nat Commun 11(1):301. https://doi.org/10.1038/s41467-019-14269-w
Chaisson MJP, Sanders AD, Zhao X, Malhotra A, Porubsky D, Rausch T et al (2019) Multi-platform discovery of haplotype-resolved structural variation in human genomes. Nat Commun 10(1):1784. https://doi.org/10.1038/s41467-018-08148-z
Cooke SB, Klukkert S (2023, this volume) Diet, dentition and jaw shape in Aotus. In: Fernandez-Duque E (ed) Owl Monkeys. Biology, Adaptive Radiation, and Behavioral Ecology of the Only Nocturnal Primate in the Americas. Springer, Cham
de Manuel M, Kuhlwilm M, Frandsen P, Sousa VC, Desai T, Prado-Martinez J et al (2016) Chimpanzee genomic diversity reveals ancient admixture with bonobos. Science 354(6311):477–481. https://doi.org/10.1126/science.aag2602
Dennis MY, Nuttle X, Sudmant PH, Antonacci F, Graves TA, Nefedov M et al (2012) Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell 149(4):912–922. https://doi.org/10.1016/j.cell.2012.03.033
DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C et al (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43(5):491–498. https://doi.org/10.1038/ng.806
Di Fiore A, Valencia LM, Martins A (2023, this volume) Phylogenetics and phylogeography of Owl Monkeys (Aotus): the molecular evidence. In: Fernandez-Duque E (ed) Owl Monkeys. Biology, Adaptive Radiation, and Behavioral Ecology of the Only Nocturnal Primate in the Americas. Springer, Cham
English AC, Richards S, Han Y, Wang M, Vee V, Qu J et al (2012) Mind the gap: upgrading genomes with Pacific biosciences RS long-read sequencing technology. PLoS One 7(11):e47768. https://doi.org/10.1371/journal.pone.0047768
Fernandez-Duque E, de la Iglesia H (2023) Temporal Niche Plasticity of Owl Monkeys. In: Fernandez-Duque E (ed) Owl Monkeys. Biology, Adaptive Radiation, and Behavioral Ecology of the Only Nocturnal Primate in the Americas. Springer, Cham
Fernandez-Duque E, Juárez CP, Defler TR (2023) Morphology, Systematics and Taxonomy of Owl Monkeys. In: Fernandez-Duque E (ed) Owl Monkeys. Biology, Adaptive Radiation, and Behavioral Ecology of the Only Nocturnal Primate in the Americas. Springer, Cham
Figueiro HV, Li G, Trindade FJ, Assis J, Pais F, Fernandes G et al (2017) Genome-wide signatures of complex introgression and adaptive evolution in the big cats. Sci Adv 3(7):e1700299. https://doi.org/10.1126/sciadv.1700299
Fleagle JG (2013) Primate adaptation and evolution, 3rd ed, 3rd edn. Academic Press, New York
Garcia de la Chica A, Spence-Aizenberg A, Wolovich CK, Evans S, Fernandez-Duque E (2023, this volume) Social behavior in Owl Monkeys. In: Fernandez-Duque E (ed) Owl Monkeys. Biology, Adaptive Radiation, and Behavioral Ecology of the Only Nocturnal Primate in the Americas. Springer, Cham
Gnerre S, Maccallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ et al (2011) High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci U S A 108(4):1513–1518. https://doi.org/10.1073/pnas.1017351108
Guevara EE, Webster TH, Lawler RR, Bradley BJ, Greene LK, Ranaivonasy J et al (2021) Comparative genomic analysis of sifakas (Propithecus) reveals selection for folivory and high heterozygosity despite endangered status. Sci Adv 7(17). https://doi.org/10.1126/sciadv.abd2274
Harris RA, Tardif SD, Vinar T, Wildman DE, Rutherford JN, Rogers J et al (2014) Evolutionary genetics and implications of small size and twinning in callitrichine primates. Proc Natl Acad Sci U S A 111(4):1467–1472. https://doi.org/10.1073/pnas.1316037111
He Y, Luo X, Zhou B, Hu T, Meng X, Audano PA et al (2019) Long-read assembly of the Chinese rhesus macaque genome and identification of ape-specific structural variants. Nat Commun 10(1):4233. https://doi.org/10.1038/s41467-019-12174-w
Hejase HA, Dukler N, Siepel A (2020) From summary statistics to gene trees: methods for inferring positive selection. Trends Genet 36(4):243–258. https://doi.org/10.1016/j.tig.2019.12.008
Hikishima K, Ando K, Komaki Y, Kawai K, Yano R, Inoue T et al (2015) Voxel-based morphometry of the marmoset brain: in vivo detection of volume loss in the substantia nigra of the MPTP-treated Parkinson's disease model. Neuroscience 300:585–592. https://doi.org/10.1016/j.neuroscience.2015.05.041
Kovner R, Souaiaia T, Fox AS, French DA, Goss CE, Roseboom PH et al (2020) Transcriptional profiling of primate central nucleus of the Amygdala neurons to understand the molecular underpinnings of early-life anxious temperament. Biol Psychiatry 88(8):638–648. https://doi.org/10.1016/j.biopsych.2020.05.009
Krienen FM, Goldman M, Zhang QR, Florio CHDR, Machold M et al (2020) Innovations present in the primate interneuron repertoire. Nature 586(7828):262–269. https://doi.org/10.1038/s41586-020-2781-z
Kronenberg ZN, Fiddes IT, Gordon D, Murali S, Cantsilieris S, Meyerson OS et al (2018) High-resolution comparative analysis of great ape genomes. Science 360(6393). https://doi.org/10.1126/science.aar6343
Kuang W, Hu J, Wu H, Fen X, Dai Q, Fu Q et al (2020) Genetic diversity, inbreeding level, and genetic load in endangered snub-nosed monkeys (Rhinopithecus). Front Genet 11:615926. https://doi.org/10.3389/fgene.2020.615926
Li H. (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997v2
Link A, Munoz-Delgado J, Montilla S (2023, this volume). Nocturnality and Activity Budgets of Owl Monkeys in Tropical Ecosystems. In: Fernandez-Duque E (ed) Owl Monkeys. Biology, Adaptive Radiation, and Behavioral Ecology of the Only Nocturnal Primate in the Americas. Springer, Cham
Liu Z, Zhang L, Yan Z, Ren Z, Han F, Tan X et al (2020) Genomic mechanisms of physiological and morphological adaptations of Limestone Langurs to Karst habitats. Mol Biol Evol 37(4):952–968. https://doi.org/10.1093/molbev/msz301
Ma NS, Aquino R, Collins WE (1985) Two new karyotypes in the Peruvian owl monkey (Aotus trivirgatus). Am J Primatol 9(4):333–341. https://doi.org/10.1002/ajp.1350090409
Mahmoud M, Gobet N, Cruz-Davalos DI, Mounier N, Dessimoz C, Sedlazeck FJ (2019) Structural variant calling: the long and the short of it. Genome Biol 20(1):246. https://doi.org/10.1186/s13059-019-1828-7
Mattle-Greminger MP, Bilgin Sonay T, Nater A, Pybus M, Desai T, de Valles G et al (2018) Genomes reveal marked differences in the adaptive evolution between orangutan species. Genome Biol 19(1):193. https://doi.org/10.1186/s13059-018-1562-6
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A et al (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20(9):1297–1303. https://doi.org/10.1101/gr.107524.110
Menezes AN, Bonvicino CR, Seuanez HN (2010) Identification, classification and evolution of owl monkeys (Aotus, Illiger 1811). BMC Evol Biol 10:248. https://doi.org/10.1186/1471-2148-10-248
Park JE, Silva AC (2019) Generation of genetically engineered non-human primate models of brain function and neurological disorders. Am J Primatol 81(2):e22931. https://doi.org/10.1002/ajp.22931
Prado-Martinez J, Sudmant PH, Kidd JM, Li H, Kelley JL, Lorente-Galdos B et al (2013) Great ape genetic diversity and population history. Nature 499(7459):471–475. https://doi.org/10.1038/nature12228
Rogers J (2018) The behavioral genetics of nonhuman primates: status and prospects. Am J Phys Anthropol 165(Suppl 65):23–36. https://doi.org/10.1002/ajpa.23384
Rogers J, Raveendran M, Fawcett GL, Fox AS, Shelton SE, Oler JA et al (2013) CRHR1 genotypes, neural circuits and the diathesis for anxiety and depression. Mol Psychiatry 18(6):700–707. https://doi.org/10.1038/mp.2012.152
Rogers J, Raveendran M, Harris RA, Mailund T, Leppala K, Athanasiadis G et al (2019) The comparative genomics and complex population history of Papio baboons. Sci Adv 5(1):eaau6947. https://doi.org/10.1126/sciadv.aau6947
Rosenberger AL, Tejedor MF (2023, this volume) Why Owl Monkeys are Pitheciids: morphology, adaptations and the evolutionary history of the Aotus lineage. In: Fernandez-Duque E (ed) Owl Monkeys. Biology, Adaptive Radiation, and Behavioral Ecology of the Only Nocturnal Primate in the Americas. Springer, Cham
Seppey M, Manni M, Zdobnov EM (2019) BUSCO: assessing genome assembly and annotation completeness. Methods Mol Biol 1962:227–245. https://doi.org/10.1007/978-1-4939-9173-0_14
Sharma G, Huo A, Kimura T, Shiozawa S, Kobayashi R, Sahara N et al (2019) Tau isoform expression and phosphorylation in marmoset brains. J Biol Chem 294(30):11433–11444. https://doi.org/10.1074/jbc.RA119.008415
Spence-Aizenberg A, Evans S, Wolovich C, Larson S, Fernandez-Duque E, Williams L (2023, this volume) Aotus: a model to synthesize studies of captive and wild primates. In: Fernandez-Duque E (ed) Owl Monkeys. Biology, Adaptive Radiation, and Behavioral Ecology of the Only Nocturnal Primate in the Americas. Springer, Cham
Svardal H, Jasinska AJ, Apetrei C, Coppola G, Huang Y, Schmitt CA et al (2017) Ancient hybridization and strong adaptation to viruses across African vervet monkey populations. Nat Genet. https://doi.org/10.1038/ng.3980
Thomas GWC, Wang RJ, Puri A, Harris RA, Raveendran M, Hughes DST et al (2018) Reproductive longevity predicts mutation rates in primates. Curr Biol 28(19):3193–3197 e3195. https://doi.org/10.1016/j.cub.2018.08.050
Veilleux CC, Heesy CP (2023) Visual system of the only nocturnal anthropoid, Aotus: the owl monkey. In: Fernandez-Duque E (ed) Owl Monkeys. Biology, Adaptive Radiation, and Behavioral Ecology of the Only Nocturnal Primate in the Americas. Springer, Cham
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S et al (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9(11):e112963. https://doi.org/10.1371/journal.pone.0112963
Wang L, Wu J, Liu X, Di D, Liang Y, Feng Y et al (2019) A high-quality genome assembly for the endangered golden snub-nosed monkey (Rhinopithecus roxellana). Gigascience 8(8). https://doi.org/10.1093/gigascience/giz098
Warren WC, Harris RA, Haukness M, Fiddes IT, Murali SC, Fernandes J et al (2020) Sequence diversity analyses of an improved rhesus macaque genome enhance its biomedical utility. Science 370(6523). https://doi.org/10.1126/science.abc6617
Xue C, Raveendran M, Harris RA, Fawcett GL, Liu X, White S et al (2016) The population genomics of rhesus macaques (Macaca mulatta) based on whole-genome sequences. Genome Res 26(12):1651–1662. https://doi.org/10.1101/gr.204255.116
Yu L, Wang GD, Ruan J, Chen YB, Yang CP, Cao X et al (2016) Genomic analysis of snub-nosed monkeys (Rhinopithecus) identifies genes and processes related to high-altitude adaptation. Nat Genet 48(8):947–952. https://doi.org/10.1038/ng.3615
Zhou X, Wang B, Pan Q, Zhang J, Kumar S, Sun X et al (2014) Whole-genome sequencing of the snub-nosed monkey provides insights into folivory and evolutionary history. Nat Genet 46(12):1303–1310. https://doi.org/10.1038/ng.3137
Acknowledgments
We thank Harsha Doppapaneni and Donna M. Muzny for overseeing the production of Aotus sequence data at HGSC and Daniel Hughes and Shwetha Murali for their assistance with the genome assembly analyses. We also thank Eric Vallender and Hazel Byrne for their helpful comments on an earlier version of this manuscript. Partial funding for the sequencing of the reference animal was provided by NIH-NIAID contract HHSN272201200031C to Mary Galinski (Emory University). The Indiana University Precision Health Initiative provided partial support for the sequencing of the 30 additional A. nancymaae individuals through a grant to Matthew Hahn (Indiana University).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 Eduardo Fernandez-Duque
About this chapter
Cite this chapter
Rogers, J., Harris, R.A., Raveendran, M., Williams, L., Worley, K.C. (2023). A Reference Genome Assembly and Initial Polymorphism Data for Aotus nancymaae. In: Fernandez-Duque, E. (eds) Owl Monkeys. Developments in Primatology: Progress and Prospects. Springer, Cham. https://doi.org/10.1007/978-3-031-13555-2_8
Download citation
DOI: https://doi.org/10.1007/978-3-031-13555-2_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-13554-5
Online ISBN: 978-3-031-13555-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)