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17 - Gibbon Phylogenetics and Genomics

Published online by Cambridge University Press:  13 April 2023

By
Lucia Carbone ,
Mariam Okhovat  and
Christian Roos
Edited by
Susan M. Cheyne ,
Carolyn Thompson ,
Peng-Fei Fan  and
Helen J. Chatterjee
Susan M. Cheyne
Affiliation:
Borneo Nature Foundation
Carolyn Thompson
Affiliation:
University College London
Peng-Fei Fan
Affiliation:
Sun Yat-Sen University, China
Helen J. Chatterjee
Affiliation:
University College London
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Summary

The gibbons (family Hylobatidae) occupy a key node in the primate phylogenetic tree. They are characterised by an accelerated rate of evolutionary chromosomal rearrangements. To date, despite much effort, the phylogeny of gibbons remains largely unresolved at the genus level, likely due to rapid divergence of the four genera approximately 5 million years ago. In this chapter we discuss various approaches used to untangle the complex phylogeny of the gibbons. We highlight the unique branching pattern of the gibbon tree, which suggests that the four genera diverged over short evolutionary time. Furthermore, we review how cutting-edge DNA sequencing technologies have improved our understanding of the evolution of the gibbon genome and how this can guide conservation efforts. In particular, we describe the mechanisms that have contributed to the highly rearranged karyotypes of the gibbon genera and how the birth and consequent propagation of the gibbon-specific transposable element LAVA might have shaped the evolution of this lineage by inserting within nearby genes involved in chromosome segregation and DNA repair. As more genetic resources and data are generated from gibbon species, we will gain further insight into the evolutionary history and enable progress towards generating greater infrastructures to conserve these threatened species.

Keywords

gibbon generagenomephylogenychromosomeskaryotypetransposable elements
Type
Chapter
Information
Gibbon Conservation in the Anthropocene , pp. 286 - 301
Publisher: Cambridge University Press
Print publication year: 2023

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References

Anandam, M.V., Groves, C.P., Molur, S., et al. (2013). Species accounts of Hylobatidae. In Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. (eds.), Handbook of the Mammals of the World, Vol. 3. Primates. Lynx Edicions, Barcelona: 778–791.Google Scholar
Bailey, W.J., Fitch, D.H., Tagle, D.A., et al. (1991). Molecular evolution of the psi eta-globin gene locus: gibbon phylogeny and the hominoid slowdown. Molecular Biology and Evolution, 8: 155–184.Google Scholar
Biegert, J. (1973). Dermatoglyphics in gibbons and siamangs. In Rumbaugh, D.M. (ed.), Gibbon and Siamang. Karger, Basel: 163–184.Google Scholar
Brandon-Jones, D., Eudey, A.A., Geissmann, T., et al. (2004). Asian primate classification. International Journal of Primatology, 25: 97–164.Google Scholar
Brockelman, W.Y. and Gittins, S.P. (1984). Natural hybridization in the Hylobates lar species group: implications for speciation in gibbons. In Preuschoft, H., Chivers, D.J., Brockelman, W.Y. and Creel, N. (eds.), The Lesser Apes: Evolutionary and Behavioural Biology. Edinburgh University Press, Edinburgh: 498–532.Google Scholar
Cane, M.A. and Molnar, P. (2001). Closing of the Indonesian seaway as a precursor to east African aridification around 3–4 million years ago. Nature, 411(6834): 157–162.Google Scholar
Capozzi, O., Carbone, L., Stanyon, R.R., et al. (2012). A comprehensive molecular cytogenetic analysis of chromosome rearrangements in gibbons. Genome Research, 22(12): 2520–2528.Google Scholar
Carbone, L., Vessere, G.M., Hallers, B.F., et al. (2006). A high-resolution map of synteny disruptions in gibbon and human genomes. PLoS Genetics, 2(12): e223.Google Scholar
Carbone, L., Harris, R.A., Vessere, G.M., et al. (2009a). Evolutionary breakpoints in the gibbon suggest association between cytosine methylation and karyotype evolution. PLoS Genetics, 5(6): e1000538.Google Scholar
Carbone, L., Mootnick, A.R., Nadler, T., et al. (2009b). A chromosomal inversion unique to the northern white-cheeked gibbon. PLoS ONE, 4(3): e4999.Google Scholar
Carbone, L., Harris, R.A., Mootnick, A.R., et al. (2012). Centromere remodeling in Hoolock leuconedys (Hylobatidae) by a new transposable element unique to the gibbons. Genome Biology and Evolution, 4: 648–658.Google Scholar
Carbone, L., Harris, R.A., Gnerre, S., et al. (2014). The gibbon genome provides a novel perspective on the accelerated karyotype evolution of small apes. Nature, 513: 195–201.Google Scholar
Chan, Y.C., Roos, C., Inoue-Murayama, M., et al. (2010). Mitochondrial genome sequences effectively reveal the phylogeny of Hylobates gibbons. PLoS ONE, 5(12): e14419.Google Scholar
Chan, Y.C., Roos, C., Inoue-Murayama, M., et al. (2012). A comparative analysis of Y chromosome and mtDNA phylogenies of the Hylobates gibbons. BMC Evolutionary Biology, 12: 150.Google Scholar
Chan, Y.C., Roos, C., Inoue-Murayama, M., et al. (2013). Inferring the evolutionary histories of divergences in Hylobates and Nomascus gibbons through multilocus sequence data. BMC Evolutionary Biology, 13: 82.Google Scholar
Chatterjee, H.J., Ho, S.Y., Barnes, I. and Groves, C. (2009). Estimating the phylogeny and divergence times of primates using a supermatrix approach. BMC Evolutionary Biology, 9: 259.Google Scholar
Chivers, D.J. (1977). The lesser apes. In Prince Rainier III of Monaco and Bourne, G.H. (eds.), Primate Conservation. Academic Press, New York: 539–598.Google Scholar
Chivers, D.J. (2013). Family Hylobatidae (gibbons). In Mittermeier, R.A., Rylands, A.B. and Wilson, D.E. (eds.), Handbook of the Mammals of the World, Vol. 3. Primates. Lynx Edicions, Barcelona: 754–777.Google Scholar
Choudhury, A. (2013). Description of a new subspecies of hoolock gibbon Hoolock hoolock from northeast India. Newsletter and Journal of the Rhino Foundation for Nature in Northeast India, 9: 49–59.Google Scholar
Cordaux, R. and Batzer, M.A. (2009). The impact of retrotransposons on human genome evolution. Nature Reviews Genetics, 10(10): 691–703.Google Scholar
Creel, N. and Preuschoft, H. (1984). Systematics of the lesser apes: a quantitative taxonomic analysis of craniometric and other variables. In Preuschoft, H., Chivers, D.J., Brockelman, W.Y. and Creel, N. (eds.), The Lesser Apes: Evolutionary and Behavioural Biology. Edinburgh University Press, Edinburgh: 562–613.Google Scholar
Darga, L.L., Baba, M.L., Weiss, M.L. and Goodman, M. (1984). Molecular perspectives on the evolution of the lesser apes. In Preuschoft, H., Chivers, D.J., Brockelman, W.Y. and Creel, N. (eds.), The Lesser Apes: Evolutionary and Behavioural Biology. Edinburgh University Press, Edinburgh: 448–466.Google Scholar
Dene, H.T., Goodman, M. and Prychodko, W. (1976). Immunodiffusion evidence on the phylogeny of the primates. In Goodman, M., Tashian, R.E. and Tashian, J.H. (eds.), Molecular Anthropology: Genes and Proteins in the Evolutionary Ascent of the Primates. Plenum Press, New York: 171–195.Google Scholar
Fabre, P.H., Rondrigues, A. and Douzery, E.J. (2009). Patterns of macroevolution among primates inferred from a supermatrix approach of mitochondrial and nuclear DNA. Molecular Phylogenetics and Evolution, 53: 808–825.Google Scholar
Fan, P.-F., He, K., Chen, X., et al. (2017). Description of a new Hoolock gibbon (Primates: Hylobatidae) based on integrative taxonomy. American Journal of Primatology, 79: e22631.Google Scholar
Felsenstein, J. (1987). Estimation of hominoid phylogeny from a DNA hybridization data set. Journal of Molecular Evolution, 26: 123–131.Google Scholar
Finstermeier, K., Zinner, D., Brameier, M., et al. (2013). A mitogenomic phylogeny of living primates. PLoS ONE, 8(7): e69504.Google Scholar
Fleagle, J.G. (1999). Primate Adaptation and Evolution. Academic Press, New York.Google Scholar
Garza, J.C. and Woodruff, D.S. (1992). A phylogenetic study of the gibbons (Hylobatidae) using DNA obtained noninvasively from hair. Molecular Phylogenetics and Evolution, 1: 202–210.Google Scholar
Geissmann, T. (1989). A female black gibbon, Hylobates concolor subspecies, from northeastern Vietnam. International Journal of Primatology, 10: 455–476.Google Scholar
Geissmann, T. (1993). Evolution of communication in gibbons (Hylobatidae). PhD thesis, Anthropological Institute, Zurich University.Google Scholar
Geissmann, T. (1995). Gibbon systematics and species identification. International Zoo News, 42: 467–501.Google Scholar
Geissmann, T. (2002a). Duet-splitting and the evolution of gibbon songs. Biological Reviews, 77: 57–76.Google Scholar
Geissmann, T. (2002b). Taxonomy and evolution of gibbons. In Soligo, C., Anzenberger, G. and Martin, R.D. (eds.), Anthropology and Primatology into the Third Millennium: The Centenary Congress of the Zurich Anthropological Institute. Wiley-Liss, New York: 28–31.Google Scholar
Geissmann, T. (2007). Status reassessment of the gibbons: results of the Asian Primate Red List workshop 2006. Gibbon Journal, 3: 5–15.Google Scholar
Geissmann, T., Dang, N.X., Lormée, N. and Momberg, F. (2000). Vietnam Primate Conservation Status Review 2000. Part 1: Gibbons. Fauna and Flora International, Hanoi, Vietnam.Google Scholar
Girirajan, S., Chen, L., Graves, T., et al. (2009). Sequencing human–gibbon breakpoints of synteny reveals mosaic new insertions at rearrangement sites. Genome Research, 19(2): 178–190.Google Scholar
Goldman, D., Giri, P.R. and O’Brien, S.J. (1987). A molecular phylogeny of the hominoid primates as indicated by two-dimensional protein electrophoresis. Proceedings of the National Academy of Sciences USA, 84: 3307–3311.Google Scholar
Goodman, M., Tagle, D.A., Fitch, D.H.A., et al. (1990). Primate evolution at the DNA level and a classification of hominoids. Journal of Molecular Evolution, 30: 260–266.Google Scholar
Goodman, M., Porter, C.A., Czelusniak, J., et al. (1998). Toward a phylogenetic classification of primates based on DNA evidence complemented by fossil evidence. Molecular Phylogenetics and Evolution, 9: 585–598.Google Scholar
Groves, C.P. (1972). Systematics and phylogeny of gibbons. In Rumbaugh, D.M. (ed.), Gibbon and Siamang, Vol. 1. Karger, Basel: 1–89.Google Scholar
Groves, C.P. (1984). A new look at the taxonomy and phylogeny of the gibbons. In Preuschoft, H., Chivers, D.J., Brockelman, W.Y. and Creel, N. (eds.), The Lesser Apes: Evolutionary and Behavioural Biology. Edinburgh University Press, Edinburgh: 542–561.Google Scholar
Groves, C.P. (1989). A Theory of Human and Primate Evolution. Clarendon Press, Oxford.Google Scholar
Groves, C.P. (1993). Speciation in living hominoid primates. In Kimbel, W.H. and Martin, L.B. (eds.), Species, Species Concepts, and Primate Evolution. Plenum Press, New York: 109–121.Google Scholar
Groves, C.P. (2001). Primate Taxonomy. Smithsonian Institution Press, Washington, DC.Google Scholar
Groves, C.P. and Wang, Y. (1990). The gibbons of the subgenus Nomascus (Primates, Mammalia). Zoological Research, 11: 147–154.Google Scholar
Haimoff, E.H., Chivers, D.J., Gittens, S.P. and Whitten, A.J. (1982). A phylogeny of gibbons (Hylobates spp.) based on morphological and behavioural characters. Folia Primatologica, 39: 213–237.Google Scholar
Hall, L.M., Jones, D.S. and Wood, B.A. (1998). Evolution of the gibbon subgenera inferred from cytochrome b DNA sequence data. Molecular Phylogenetics and Evolution, 10: 281–286.Google Scholar
Hayashi, S., Hayasaka, K., Takenaka, O. and Horai, S. (1995). Molecular phylogeny of gibbons inferred from mitochondrial DNA sequences: preliminary report. Journal of Molecular Evolution, 41: 359–365.Google Scholar
Hellekant, G., DuBois, G., Geissmann, T., Glaser, D. and Van der Weel, H. (1990). Taste responses of chorda tympani proper nerve in the white-handed gibbon (Hylobates lar). In Døving, K.B. (ed.), Proceedings of the Tenth International Symposium on Olfaction and Taste, University of Oslo, Norway, July 16–20, 1989. GCS (Graphic Communication System), Oslo: 115–131.Google Scholar
Israfil, H., Zehr, S.M., Mootnick, A.R., Ruvolo, M. and Steiper, M.E. (2011). Unresolved molecular phylogenies of gibbons and siamangs (family: Hylobatidae) based on mitochondrial, Y-linked, and X-linked loci indicate a rapid Miocene radiation or sudden vicariance event. Molecular Phylogenetics and Evolution, 58: 447–455.Google Scholar
Jauch, A., Wienberg, J., Stanyon, R., et al. (1992). Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting. Proceedings of the National Academy of Sciences USA, 89(18): 8611–8615.Google Scholar
Kim, S.K., Carbone, L., Becquet, C., et al. (2011). Patterns of genetic variation within and between gibbon species. Molecular Biology and Evolution, 28: 2211–2218.Google Scholar
Koehler, U., Arnold, N., Wienberg, J., Tofanelli, S. and Stanyon, R. (1995). Genomic reorganization and disrupted chromosomal synteny in the siamang (Hylobates syndactylus) revealed by fluorescence in situ hybridization. Americal Journal of Physical Anthropology, 97(1): 37–47.Google Scholar
Konrad, R. and Geissmann, T. (2006). Vocal diversity and taxonomy of Nomascus in Cambodia. International Journal of Primatology, 27: 713–745.Google Scholar
Lanciano, S. and Cristofari, G. (2020). Measuring and interpreting transposable element expression. Nature Reviews Genetics, 21: 721–736.Google Scholar
Liu, R., Shi, L. and Chen, Y. (1987). [A study on the chromosomes of white-browed gibbon (Hylobates hoolock leuconedys)]. Acta Theriologica Sinica, 7: 1–7. (Chinese text, English summary)Google Scholar
Ma, S. and Wang, Y. (1986). The taxonomy and distribution of the gibbons in southern China and its adjacent region, with description of three new subspecies. Zoological Research, 7: 393–410.Google Scholar
Marshall, J.T. and Sugardjito, J. (1986). Gibbon systematics. In Swindler, D.R. and Erwin, J. (eds.), Comparative Primate Biology, Vol. 1. Systematics, Evolution, and Anatomy. Alan R. Liss, New York: 137–185.Google Scholar
Matsudaira, K. and Ishida, T. (2010). Phylogenetic relationships and divergence dates of the whole mitochondrial genome sequences among three gibbon genera. Molecular Phylogenetics and Evolution, 54: 33–37.Google Scholar
Matsudaira, K. and Ishida, T. (2020). Divergence and introgression in small apes, the genus Hylobates, revealed by reduced representation sequencing. Heredity, 127: 312–322.Google Scholar
Meyer, T.J., McLain, A.T., Oldenburg, J.M., et al. (2012). An Alu-based phylogeny of gibbons (Hylobatidae). Molecular Biology and Evolution, 29: 3441–3450.Google Scholar
Misceo, D., Capozzi, O., Roberto, R., et al. (2008). Tracking the complex flow of chromosome rearrangements from the Hominoidea ancestor to extant gibbons Nomascus and Hylobates by high-resolution synteny mapping. Genome Research, 18: 1530–1537.Google Scholar
Monda, K., Simmons, R.E., Kressirer, P., Su, B. and Woodruff, D.S. (2007). Mitochondrial DNA hypervariable Region-1 sequence variation and phylogeny of the concolor gibbons, Nomascus. American Journal of Primatology, 69: 1–22.Google Scholar
Mootnick, A.R. (2006). Gibbon (Hylobatidae) species identification recommended for rescue or breeding centers. Primate Conservation, 21: 103–138.Google Scholar
Mootnick, A.R. and Fan, P. (2011). A comparative study of crested gibbons (Nomascus). American Journal of Primatology, 73: 135–154.Google Scholar
Mootnick, A.R. and Groves, C.P. (2005). A new generic name for the hoolock gibbon (Hylobatidae). International Journal of Primatology, 26: 971–976.Google Scholar
Müller, S., Hollatz, M. and Wienberg, J. (2003). Chromosomal phylogeny and evolution of gibbons (Hylobatidae). Human Genetics, 113: 493–501.Google Scholar
Napier, J.R. and Napier, P.H. (1967). A Handbook of Living Primates: Morphology, Ecology and Behaviour of Nonhuman Primates. Academic Press, London.Google Scholar
Okhovat, M., Nevonen, K.A., Davis, B.A., et al. (2020). Co-option of the lineage-specific LAVA retrotransposon in the gibbon genome. Proceedings of the National Academy of Sciences USA, 117(32): 19328–19338.Google Scholar
Perelman, P., Johnson, W.E., Roos, C., et al. (2011). A molecular phylogeny of living primates. PLoS Genetics, 7: e1001342.Google Scholar
Prouty, L.A., Buchanan, P.D., Pollitzer, W.S. and Mootnick, A.R. (1983). Bunopithecus: a genus-level taxon for the hoolock gibbon (Hylobates hoolock). American Journal of Primatology, 5: 83–87.Google Scholar
Rawson, B.M., Insua-Cao, P., Ha, N.M., et al. (2011). The Conservation Status of Gibbons in Vietnam. Fauna and Flora International and Conservation International, Hanoi, Vietnam.Google Scholar
Ray, D.A., Xing, J., Hedges, D.J., et al. (2005). Alu insertion loci and platyrrhine primate phylogeny. Molecular Phylogenetics and Evolution, 35(1): 117–126.Google Scholar
Remane, A. (1921). Beiträge zur Morphologie des Anthropoidengebisses. Wiegmann-Archiv für Naturgeschichte, 87: 1–179.Google Scholar
Roberto, R., Capozzi, O., Wilson, R.K., et al. (2007). Molecular refinement of gibbon genome rearrangements. Genome Research, 17(2): 249–257.Google Scholar
Roos, C. (2004). Molecular evolution and systematics of Vietnamese primates. In Nadler, T., Streicher, U. and Long, H.T. (eds.), Conservation of Primates in Vietnam. Frankfurt Zoological Society, Hanoi, Vietnam: 23–28.Google Scholar
Roos, C. and Geissmann, T. (2001). Molecular phylogeny of the major hylobatid divisions. Molecular Phylogenetics and Evolution, 19: 486–494.Google Scholar
Roos, C., Schmitz, J. and Zischler, H. (2004). Primate jumping genes elucidate strepsirrhine phylogeny. Proceedings of the National Academy of Sciences USA, 101(29): 10650–10654.Google Scholar
Roos, C., Thanh, V.N., Walter, L. and Nadler, T. (2007). Molecular sytematics of Indochinese primates. Vietnamese Journal of Primatology, 1: 41–53.Google Scholar
Roos, C., Boonratana, R., Supriatna, J., et al. (2014). An updated taxonomy and conservation status review of Asian primates. Asian Primates Journal, 4: 2–38.Google Scholar
Rowe, N. (1996). The Pictorial Guide to the Living Primates. Pogonias Press, New York.Google Scholar
Rowe, N. and Myers, M. (2016). All the World’s Primates. Pogonias Press, New York.Google Scholar
Ruppell, J. (2007). The gibbons of Phong Nha-Ke Bang National Park. Gibbon Journal, 3: 50–55.Google Scholar
Salem, A.H., Ray, D.A., Xing, J., et al. (2003). Alu elements and hominid phylogenetics. Proceedings of the National Academy of Sciences USA, 100: 12787–12791.Google Scholar
Sarich, V.M. and Cronin, J.E. (1976). Molecular systematics of the primates. In Goodman, M., Tashian, R.E. and Tashian, J.H. (eds.), Molecular Anthropology: Genes and Proteins in the Evolutionary Ascent of the Primates. Plenum Press, New York: 141–170.Google Scholar
Sasaki, T., Takahashi, K., Nikaido, M., et al. (2004). First application of the SINE (short interspersed repetitive element) method to infer phylogenetic relationships in reptiles: an example from the turtle superfamily Testudinoidea. Molecular Biology and Evolution, 21(4): 705–715.Google Scholar
Sawalischin, M. (1911). Der Musculus flexor communis brevis digitorum pedis in der Primatenreihe, mit spezieller Berücksichtigung der menschlichen Varietäten. Morphologisches Jahrbuch, 42: 557–663.Google Scholar
Schultz, A.H. (1933). Observations on the growth, classification and evolutionary specialization of gibbons and siamangs. Human Biology, 5: 212–255, 385–428.Google Scholar
Schultz, A.H. (1973). The skeleton of the Hylobatidae and other observations on their morphology. In Rumbaugh, D.M. (ed.), Gibbon and Siamang. Karger, Basel: 1–54.Google Scholar
Shi, C.-M. and Yang, Z. (2018). Coalescent-based analyses of genomic sequence data provide a robust resolution of phylogenetic relationships among major groups of gibbons. Molecular Biology and Evolution, 35: 159–179.Google Scholar
Sibley, C.G. and Ahlquist, J.E. (1984). The phylogeny of hominoid primates, as indicated by DNA–DNA hybridization. Journal of Molecular Evolution, 20: 2–15.Google Scholar
Sibley, C.G. and Ahlquist, J.E. (1987). DNA hybridization evidence of hominoid phylogeny: results from an expanded data set. Journal of Molecular Evolution, 26: 99–121.Google Scholar
Simonetta, A. (1957). Catalogo e sinonimia annotata degli ominoidi fossili ed attuali (1758–1955). Atti della Società Toscana di Scienze Naturali, Memorie Serie B, 64: 53–113.Google Scholar
Stanyon, R. (2013). Cytogenetic studies of small ape (Hylobatidae) chromosomes. Tsitologiia, 55: 167–171.Google Scholar
Takacs, Z., Morales, J.C., Geissmann, T. and Melnick, D.J. (2005). A complete species-level phylogeny of the Hylobatidae based on mitochondrial ND3-ND4 gene sequences. Molecular Phylogenetics and Evolution, 36: 456–467.Google Scholar
Thinh, V.N., Mootnick, A.R., Geissmann, T., et al. (2010a). Mitochondrial evidence for multiple radiations in the evolutionary history of small apes. BMC Evolutionary Biology, 10: 74.Google Scholar
Thinh, V.N., Mootnick, A.R., Thanh, V.N., Nadler, T. and Roos, C. (2010b). A new species of crested gibbon, from the Central Annamite Mountain Range. Vietnamese Journal of Primatology, 4: 1–12.Google Scholar
Thinh, V.N., Rawson, B., Hallam, C., et al. (2010c). Phylogeny and distribution of crested gibbons (genus Nomascus) based on mitochondrial cytochrome b gene sequence data. American Journal of Primatology, 72: 1047–1054.Google Scholar
Thinh, V.N., Hallam, C., Roos, C. and Hammerschmidt, K. (2011). Concordance between vocal and genetic diversity in crested gibbons. BMC Evolutionary Biology, 11: 36.Google Scholar
Tien, D.V. (1983). On the north Indochinese gibbons (Hylobates concolor) (Primates: Hylobatidae) in north Vietnam. Journal of Human Evolution, 12: 367–372.Google Scholar
Trizzino, M., Park, Y. Holsbach-Beltrame, M., et al. (2017). Transposable elements are the primary source of novelty in primate gene regulation. Genome Research, 27(10): 1623–1633.Google Scholar
Veeramah, K.R., Woerner, A.E., Johnstone, L., et al. (2015). Examining phylogenetic relationships among gibbon genera using whole genome sequence data using an Approximate Bayesian Computation approach. Genetics, 200: 295–308.Google Scholar
Wall, J.D., Kim, S.K., Luca, F., et al. (2013). Incomplete lineage sorting is common in extant gibbon genera. PLoS ONE, 8(1): e53682.Google Scholar
Wienberg, J. and Stanyon, R. (1987). Fluorescent heterochromatin staining in primate chromosomes. Human Evolution, 2: 445–457.Google Scholar
Wislocki, G.B. (1929). On the placentation of primates, with a consideration of the phylogeny of the placenta. Contributions to Embryology, 20: 51–80.Google Scholar
Wislocki, G.B. (1932). On the female reproductive tract of the gorilla, with a comparison of that of other primates. Contributions to Embryology, 23: 163–204.Google Scholar

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