Skip to main content

No Evidence of Copy Number Variation in Acidic Mammalian Chitinase Genes (CHIA) in New World and Old World Monkeys

Abstract

Copy number variation may be the most common form of structural genetic variation in the genome. Numerous studies have shown that gene copy number variation can correlate with phenotypic variation, where higher copy numbers correspond to increased expression of the protein and vice versa. Examples include some digestive enzyme genes, where variation in copy numbers and protein expression may be related to dietary differences. Increasing the expression of a digestive enzyme through higher gene copy numbers may thus be a potential mechanism for altering an organism’s digestive capabilities. I investigated copy number variation in genes coding for acidic mammalian chitinase, a chitinolytic digestive enzyme that may be used for the digestion of insect exoskeletons, in nonhuman primates with varying levels of insect consumption. I hypothesized that CHIA copy number correlates positively with level of insectivory, predicting higher copy numbers in more insectivorous primates. I assessed copy number variation with the QuantStudio 3D digital PCR platform, in a comparative sample of Old World and New World primate species (N = 10 species, one or two individuals each). Contrary to my prediction, no evidence of copy number variation was found and all species tested had two gene copies per diploid genome. These findings suggest that if acidic mammalian chitinase expression varies according to insect consumption in primates, it may be up- or downregulated through another mechanism.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  • Alonso, C., & Langguth, A. (1989). Ecologia e comportamento de Callithrix jacchus (Primates: Callitrichidae) numa ilha de floresta Atlântica. Revista Nordestina de Biologia, 6(2), 105–137.

    Google Scholar 

  • Axelsson, E., Ratnakumar, A., Arendt, M.-L., Maqbool, K., Webster, M. T., Perloski, M., Liberg, O., Arnemo, J. M., Hedhammar, Ã…., & Lindblad-Toh, K. (2013). The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature, 495(7441), 360–364.

    Article  PubMed  CAS  Google Scholar 

  • Behringer, V., Borchers, C., Deschner, T., Möstl, E., Selzer, D., & Hohmann, G. (2013). Measurements of salivary alpha amylase and salivary cortisol in hominoid primates reveal within-species consistency and between-species differences. PLoS One, 8(4), e60773.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bell, R. H. V. (1971). A grazing ecosystem in the Serengeti. Scientific American, 225(1), 86–93.

    Article  Google Scholar 

  • Bickhart, D. M., Hou, Y., Schroeder, S. G., Alkan, C., Cardone, M. F., Matukumalli, L. K., Song, J., Schnabel, R. D., Ventura, M., Taylor, J. F., Garcia, J. F., van Tassell, C. P., Sonstegard, T. S., Eichler, E. E., & Liu, G. E. (2012). Copy number variation of individual cattle genomes using next-generation sequencing. Genome Research, 22(4), 778–790.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Boot, R. G., Blommaart, E. F., Swart, E., Ghauharali-van der Vlugt, K., Bijl, N., et al (2001). Identification of a novel acidic mammalian chitinase distinct from chitotriosidase. Journal of Biological Chemistry, 276(9), 6770–6778.

    Article  PubMed  CAS  Google Scholar 

  • Boot, R. G., Bussink, A. P., Verhoek, M., de Boer, P. A. J., Moorman, A. F. M., & Aerts, J. M. F. G. (2005). Marked differences in tissue-specific expression of chitinases in mouse and man. Journal of Histochemistry and Cytochemistry, 53(10), 1283–1292.

    Article  PubMed  CAS  Google Scholar 

  • Brown, A. D., & Zunino, G. E. (1990). Dietary variability in Cebus apella in extreme habitats: Evidence for adaptability. Folia Primatologica, 54(3–4), 187–195.

    Article  CAS  Google Scholar 

  • BrzÄ™k, P., Ciminari, M. E., Kohl, K. D., Lessner, K., Karasov, W. H., & Caviedes-Vidal, E. (2013). Effect of age and diet composition on activity of pancreatic enzymes in birds. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 183(5), 685–697.

    Article  PubMed  CAS  Google Scholar 

  • Caldecott, J. O. (1986). An ecological and behavioural study of the pig-tailed macaque. Contributions to Primatology, 21, 1–259.

    Google Scholar 

  • Cantsilieris, S., & White, S. J. (2013). Correlating multiallelic copy number polymorphisms with disease susceptibility. Human Mutation, 34(1), 1–13.

    Article  PubMed  CAS  Google Scholar 

  • Chapman, C. A., & Fedigan, L. M. (1990). Dietary differences between neighboring Cebus capucinus groups: Local traditions, food availability or responses to food profitability. Folia Primatologica, 54(3–4), 177–186.

    Article  CAS  Google Scholar 

  • Cheng, Z., Ventura, M., She, X., Khaitovich, P., Graves, T., Osoegawa, K., Church, D., DeJong, P., Wilson, R. K., Pääbo, S., Rocchi, M., & Eichler, E. E. (2005). A genome-wide comparison of recent chimpanzee and human segmental duplications. Nature, 437(7055), 88–93.

    Article  PubMed  CAS  Google Scholar 

  • Clop, A., Vidal, O., & Amills, M. (2012). Copy number variation in the genomes of domestic animals. Animal Genetics, 43(5), 503–517.

    Article  PubMed  CAS  Google Scholar 

  • Crandlemire-Sacco, J. (1988). An ecological comparison of two sympatric primates: Saguinus fuscicollis and Callicebus moloch of Amazonian Peru. Primates, 29(4), 465–475.

    Article  Google Scholar 

  • Dennis, M. Y., Nuttle, X., Sudmant, P. H., Antonacci, F., Graves, T. A., Nefedov, M., Rosenfeld, J. A., Sajjadian, S., Malig, M., Kotkiewicz, H., Curry, C. J., Shafer, S., Shaffer, L. G., de Jong, P. J., Wilson, R. K., & Eichler, E. E. (2012). Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell, 149(4), 912–922.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Digby, L. J., Ferrari, S. F., & Saltzman, W. (2011). Callitrichines. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, S. K. Bearder, & R. M. Stumpf (Eds.), Primates in perspective (pp. 91–107). Oxford: Oxford University Press.

    Google Scholar 

  • Dumas, L., Kim, Y. H., Karimpour-Fard, A., Cox, M., Hopkins, J., Pollack, J. R., & Sikela, J. M. (2007). Gene copy number variation spanning 60 million years of human and primate evolution. Genome Research, 17(9), 1266–1277.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Elferink, M. G., Vallée, A. A. A., Jungerius, A. P., Crooijmans, R. P. M. A., & Groenen, M. A. M. (2008). Partial duplication of the PRLR and SPEF2 genes at the late feathering locus in chicken. BMC Genomics, 9, 391.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Enattah, N. S., Jensen, T. G. K., Nielsen, M., Lewinski, R., Kuokkanen, M., Rasinpera, H., el-Shanti, H., Seo, J. K., Alifrangis, M., Khalil, I. F., Natah, A., Ali, A., Natah, S., Comas, D., Mehdi, S. Q., Groop, L., Vestergaard, E. M., Imtiaz, F., Rashed, M. S., Meyer, B., Troelsen, J., & Peltonen, L. (2008). Independent introduction of two lactase-persistence alleles into human populations reflects different history of adaptation to milk culture. American Journal of Human Genetics, 82(1), 57–72.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fleagle, J. G. (2013). Primate adaptation and evolution, 3rd ed. San Diego: Academic Press.

  • Fontanesi, L., Beretti, F., Riggio, V., González, E. G., Dall’Olio, S., et al (2009). Copy number variation and missense mutations of the agouti signaling protein (ASIP) gene in goat breeds with different coat colors. Cytogenetic and Genome Research, 126(4), 333–347.

    Article  PubMed  CAS  Google Scholar 

  • Fontanesi, L., Dall’Olio, S., Beretti, F., Portolano, B., & Russo, V. (2011). Coat colours in the Massese sheep breed are associated with mutations in the agouti signalling protein (ASIP) and melanocortin 1 receptor (MC1R) genes. Animal, 5(1), 8–17.

    Article  PubMed  CAS  Google Scholar 

  • Garber, P. A. (1988). Diet, foraging patterns, and resource defense in a mixed species troop of Saguinus mystax and Saguinus fuscicollis in Amazonian Peru. Behaviour, 105(1), 18–34.

    Article  Google Scholar 

  • Gaulin, S. J. (1979). A Jarman/bell model of primate feeding niches. Human Ecology, 7(1), 1–20.

    Article  Google Scholar 

  • Gautier-Hion, A. (1988). Diet and dietary habits of forest guenons. In A primate radiation: Evolutionary biology of the African guenons (pp. 257–283). Cambridge: Cambridge University Press.

    Google Scholar 

  • Gazave, E., Darre, F., Morcillo-Suarez, C., Petit-Marty, N., Carreno, A., Marigorta, U. M., Ryder, O. A., Blancher, A., Rocchi, M., Bosch, E., Baker, C., Marques-Bonet, T., Eichler, E. E., & Navarro, A. (2011). Copy number variation analysis in the great apes reveals species-specific patterns of structural variation. Genome Research, 21(10), 1626–1639.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gingerich, P. D. (1980). Dental and cranial adaptations in Eocene Adapidae. Zeitschrift für Morphologie und Anthropologie, 71(2), 135–142.

    PubMed  CAS  Google Scholar 

  • Giuffra, E., Evans, G., Törnsten, A., Wales, R., Day, A., Looft, H., Plastow, G., & Andersson, L. (1999). The belt mutation in pigs is an allele at the dominant white (I/KIT) locus. Mammalian Genome, 10(12), 1132–1136.

    Article  PubMed  CAS  Google Scholar 

  • Gokcumen, O., Babb, P. L., Iskow, R. C., Zhu, Q., Shi, X., Mills, R. E., Ionita-Laza, I., Vallender, E. J., Clark, A. G., Johnson, W. E., & Lee, C. (2011). Refinement of primate copy number variation hotspots identifies candidate genomic regions evolving under positive selection. Genome Biology, 12(5), R52.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gokcumen, O., Tischler, V., Tica, J., Zhu, Q., Iskow, R. C., Lee, E., Fritz, M. H. Y., Langdon, A., Stutz, A. M., Pavlidis, P., Benes, V., Mills, R. E., Park, P. J., Lee, C., & Korbel, J. O. (2013). Primate genome architecture influences structural variation mechanisms and functional consequences. Proceedings of the National Academy of Sciences of the USA, 110(39), 15764–15769.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldstein, S. J., & Richard, A. F. (1989). Ecology of rhesus macaques (Macaca mulatta) in Northwest Pakistan. International Journal of Primatology, 10(6), 531–567.

    Article  Google Scholar 

  • Gschwind, A. R., Singh, A., Certa, U., Reymond, A., & Heckel, T. (2017). Diversity and regulatory impact of copy number variation in the primate Macaca fascicularis. BMC Genomics, 18, 144.

  • Hardwick, R. J., Machado, L. R., Zuccherato, L. W., Antolinos, S., Xue, Y., Shawa, N., Gilman, R. H., Cabrera, L., Berg, D. E., Tyler-Smith, C., Kelly, P., Tarazona-Santos, E., & Hollox, E. J. (2011). A worldwide analysis of beta-defensin copy number variation suggests recent selection of a high-expressing DEFB103 gene copy in East Asia. Human Mutation, 32(7), 743–750.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hollox, E. J., Armour, J. A. L., & Barber, J. C. K. (2003). Extensive normal copy number variation of a beta-defensin antimicrobial-gene cluster. American Journal of Human Genetics, 73(3), 591–600.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ingram, C. J. E., Mulcare, C. A., Itan, Y., Thomas, M. G., & Swallow, D. M. (2009). Lactose digestion and the evolutionary genetics of lactase persistence. Human Genetics, 124(6), 579–591.

    Article  PubMed  CAS  Google Scholar 

  • Isbell, L. A. (1998). Diet for a small primate: Insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus). American Journal of Primatology, 45(4), 381–398.

    Article  PubMed  CAS  Google Scholar 

  • Iskow, R. C., Gokcumen, O., Abyzov, A., Malukiewicz, J., Zhu, Q., Sukumar, A. T., Pai, A. A., Mills, R. E., Habegger, L., Cusanovich, D. A., Rubel, M. A., Perry, G. H., Gerstein, M., Stone, A. C., Gilad, Y., & Lee, C. (2012). Regulatory element copy number differences shape primate expression profiles. Proceedings of the National Academy of Sciences of the USA, 109(31), 12656–12661.

    Article  PubMed  PubMed Central  Google Scholar 

  • Itan, Y., Powell, A., Beaumont, M. A., Burger, J., & Thomas, M. G. (2009). The origins of lactase persistence in Europe. PLoS Computational Biology, 5(8), e1000491.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Itan, Y., Jones, B. L., Ingram, C. J., Swallow, D. M., & Thomas, M. G. (2010). A worldwide correlation of lactase persistence phenotype and genotypes. BMC Evolutionary Biology, 10(1), 36.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jacquemont, S., Reymond, A., Zufferey, F., Harewood, L., Walters, R. G., Kutalik, Z., Martinet, D., Shen, Y., Valsesia, A., Beckmann, N. D., Thorleifsson, G., Belfiore, M., Bouquillon, S., Campion, D., de Leeuw, N., de Vries, B. B. A., Esko, T., Fernandez, B. A., Fernández-Aranda, F., Fernández-Real, J. M., Gratacòs, M., Guilmatre, A., Hoyer, J., Jarvelin, M. R., Frank Kooy, R., Kurg, A., le Caignec, C., Männik, K., Platt, O. S., Sanlaville, D., van Haelst, M. M., Villatoro Gomez, S., Walha, F., Wu, B. L., Yu, Y., Aboura, A., Addor, M. C., Alembik, Y., Antonarakis, S. E., Arveiler, B., Barth, M., Bednarek, N., Béna, F., Bergmann, S., Beri, M., Bernardini, L., Blaumeiser, B., Bonneau, D., Bottani, A., Boute, O., Brunner, H. G., Cailley, D., Callier, P., Chiesa, J., Chrast, J., Coin, L., Coutton, C., Cuisset, J. M., Cuvellier, J. C., David, A., de Freminville, B., Delobel, B., Delrue, M. A., Demeer, B., Descamps, D., Didelot, G., Dieterich, K., Disciglio, V., Doco-Fenzy, M., Drunat, S., Duban-Bedu, B., Dubourg, C., el-Sayed Moustafa, J. S., Elliott, P., Faas, B. H. W., Faivre, L., Faudet, A., Fellmann, F., Ferrarini, A., Fisher, R., Flori, E., Forer, L., Gaillard, D., Gerard, M., Gieger, C., Gimelli, S., Gimelli, G., Grabe, H. J., Guichet, A., Guillin, O., Hartikainen, A. L., Heron, D., Hippolyte, L., Holder, M., Homuth, G., Isidor, B., Jaillard, S., Jaros, Z., Jiménez-Murcia, S., Joly Helas, G., Jonveaux, P., Kaksonen, S., Keren, B., Kloss-Brandstätter, A., Knoers, N. V. A. M., Koolen, D. A., Kroisel, P. M., Kronenberg, F., Labalme, A., Landais, E., Lapi, E., Layet, V., Legallic, S., Leheup, B., Leube, B., Lewis, S., Lucas, J., MacDermot, K. D., Magnusson, P., Marshall, C., Mathieu-Dramard, M., McCarthy, M. I., Meitinger, T., Antonietta Mencarelli, M., Merla, G., Moerman, A., Mooser, V., Morice-Picard, F., Mucciolo, M., Nauck, M., Coumba Ndiaye, N., Nordgren, A., Pasquier, L., Petit, F., Pfundt, R., Plessis, G., Rajcan-Separovic, E., Paolo Ramelli, G., Rauch, A., Ravazzolo, R., Reis, A., Renieri, A., Richart, C., Ried, J. S., Rieubland, C., Roberts, W., Roetzer, K. M., Rooryck, C., Rossi, M., Saemundsen, E., Satre, V., Schurmann, C., Sigurdsson, E., Stavropoulos, D. J., Stefansson, H., Tengström, C., Thorsteinsdóttir, U., Tinahones, F. J., Touraine, R., Vallée, L., van Binsbergen, E., van der Aa, N., Vincent-Delorme, C., Visvikis-Siest, S., Vollenweider, P., Völzke, H., Vulto-van Silfhout, A. T., Waeber, G., Wallgren-Pettersson, C., Witwicki, R. M., Zwolinksi, S., Andrieux, J., Estivill, X., Gusella, J. F., Gustafsson, O., Metspalu, A., Scherer, S. W., Stefansson, K., Blakemore, A. I. F., Beckmann, J. S., & Froguel, P. (2011). Mirror extreme BMI phenotypes associated with gene dosage at the chromosome 16p11.2 locus. Nature, 478(7367), 97–102.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Janiak, M. C., Chaney, M. E., & Tosi, A. J. (2018). Evolution of acidic mammalian chitinase genes (CHIA) is related to body mass and insectivory in primates. Molecular Biology and Evolution, 35(3), 607–622.

    Article  Google Scholar 

  • Jarman, P. J. (1974). The social organisation of antelope in relation to their ecology. Behaviour, 48(1), 215–267.

    Article  Google Scholar 

  • Kay, R. F. (1984). On the use of anatomical features to infer foraging behavior in extinct primates. In J. Cant & P. S. Rodman (Eds.), Adaptations for foraging in nonhuman primates (pp. 21–53). New York: Columbia University Press.

    Google Scholar 

  • Knogge, C., & Heymann, E. W. (2003). Seed dispersal by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis: Diversity and characteristics of plant species. Folia Primatologica, 74(1), 33–47.

    Article  Google Scholar 

  • Krykbaev, R., Fitz, L. J., Reddy, P. S., Winkler, A., Xuan, D., Yang, X., Fleming, M., & Wolf, S. F. (2010). Evolutionary and biochemical differences between human and monkey acidic mammalian chitinases. Gene, 452(2), 63–71.

    Article  PubMed  CAS  Google Scholar 

  • Lawrence, J. M. (2007). Understanding the pair bond in brown titi monkeys (Callicebus brunneus): Male and female reproductive interests. Ph.D. thesis, Columbia University, New York.

  • Lee, A. S., Gutiérrez-Arcelus, M., Perry, G. H., Vallender, E. J., Johnson, W. E., Miller, G. M., Korbel, J. O., & Lee, C. (2008). Analysis of copy number variation in the rhesus macaque genome identifies candidate loci for evolutionary and human disease studies. Human Molecular Genetics, 17(8), 1127–1136.

    Article  PubMed  CAS  Google Scholar 

  • Leonard, B. C., Marks, S. L., Outerbridge, C. A., Affolter, V. K., Kananurak, A., Young, A., Moore, P. F., Bannasch, D. L., & Bevins, C. L. (2012). Activity, expression and genetic variation of canine ß-defensin 103: A multifunctional antimicrobial peptide in the skin of domestic dogs. Journal of Innate Immunity, 4(3), 248–259.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lima, E. M., & Ferrari, S. F. (2003). Diet of a free-ranging group of squirrel monkeys (Saimiri sciureus) in eastern Brazilian Amazonia. Folia Primatologica, 74(3), 150–158.

    Article  Google Scholar 

  • Linzmeier, R. M., & Ganz, T. (2006). Copy number polymorphisms are not a common feature of innate immune genes. Genomics, 88(1), 122–126.

    Article  PubMed  CAS  Google Scholar 

  • Malhotra, D., & Sebat, J. (2012). CNVs: Harbingers of a rare variant revolution in psychiatric genetics. Cell, 148(6), 1223–1241.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mallott, E. K. (2016). Social, ecological, and developmental influences on fruit and invertebrate foraging strategies and gut microbial communities in white-faced capuchins (Cebus capucinus). Ph.D. thesis, University of Illinois at Urbana-Champaign.

  • Mandel, A. L., & Breslin, P. A. S. (2012). High endogenous salivary amylase activity is associated with improved glycemic homeostasis following starch ingestion in adults. Journal of Nutrition, 142(5), 853–858.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mandel, A. L., Peyrot des Gachons, C., Plank, K. L., Alarcon, S., & Breslin, P. A. S. (2010). Individual differences in AMY1 gene copy number, salivary α-amylase levels, and the perception of oral starch. PLoS One, 5(10), e13352.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marques-Bonet, T., Kidd, J. M., Ventura, M., Graves, T. A., Cheng, Z., Hillier, L. D. W., Jiang, Z., Baker, C., Malfavon-Borja, R., Fulton, L. A., Alkan, C., Aksay, G., Girirajan, S., Siswara, P., Chen, L., Cardone, M. F., Navarro, A., Mardis, E. R., Wilson, R. K., & Eichler, E. E. (2009). A burst of segmental duplications in the genome of the African great ape ancestor. Nature, 457(7231), 877–881.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McCabe, G. M., & Fedigan, L. M. (2007). Effects of reproductive status on energy intake, ingestion rates, and dietary composition of female Cebus capucinus at Santa Rosa, Costa Rica. International Journal of Primatology, 28(4), 837–851.

    Article  Google Scholar 

  • Nakagawa, N. (1989). Activity budget and diet of patas monkeys in Kala Maloue National Park, Cameroon: A preliminary report. Primates, 30(1), 27–34.

    Article  Google Scholar 

  • Narita, Y., Oda, S.-I., Takenaka, O., & Kageyama, T. (2000). Gastric digestive proteinases of the greater horseshoe bat, Rhinolophus ferrumequinum. Mammal Study, 25(1), 17–26.

    Article  Google Scholar 

  • Narita, Y., Oda, S.-I., Takenaka, O., & Kageyama, T. (2010). Lineage-specific duplication and loss of pepsinogen genes in hominoid evolution. Journal of Molecular Evolution, 70(4), 313–324.

    Article  PubMed  CAS  Google Scholar 

  • O’Brien, T. G., & Kinnaird, M. F. (1997). Behavior, diet, and movements of the Sulawesi crested black macaque (Macaca nigra). International Journal of Primatology, 18(3), 321–351.

    Article  Google Scholar 

  • Ohno, M., Kimura, M., Miyazaki, H., Okawa, K., Onuki, R., Nemoto, C., Tabata, E., Wakita, S., Kashimura, A., Sakaguchi, M., Sugahara, Y., Nukina, N., Bauer, P. O., & Oyama, F. (2016). Acidic mammalian chitinase is a proteases-resistant glycosidase in mouse digestive system. Scientific Reports, 6, 37756.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Okawa, K., Ohno, M., Kashimura, A., Kimura, M., Kobayashi, Y., Sakaguchi, M., Sugahara, Y., Kamaya, M., Kino, Y., Bauer, P. O., & Oyama, F. (2016). Loss and gain of human acidic mammalian chitinase activity by nonsynonymous SNPs. Molecular Biology and Evolution, 33(12), 3183–3193.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perry, G. H., Tchinda, J., McGrath, S. D., Zhang, J., Picker, S. R., Caceres, A. M., Iafrate, A. J., Tyler-Smith, C., Scherer, S. W., Eichler, E. E., Stone, A. C., & Lee, C. (2006). Hotspots for copy number variation in chimpanzees and humans. Proceedings of the National Academy of Sciences of the USA, 103(21), 8006–8011.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perry, G. H., Dominy, N. J., Claw, K. G., Lee, A. S., Fiegler, H., Redon, R., Werner, J., Villanea, F. A., Mountain, J. L., Misra, R., Carter, N. P., Lee, C., & Stone, A. C. (2007). Diet and the evolution of human amylase gene copy number variation. Nature Genetics, 39(10), 1256–1260.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pinto, D., Pagnamenta, A. T., Klei, L., Anney, R., Merico, D., Regan, R., Conroy, J., Magalhaes, T. R., Correia, C., Abrahams, B. S., Almeida, J., Bacchelli, E., Bader, G. D., Bailey, A. J., Baird, G., Battaglia, A., Berney, T., Bolshakova, N., Bölte, S., Bolton, P. F., Bourgeron, T., Brennan, S., Brian, J., Bryson, S. E., Carson, A. R., Casallo, G., Casey, J., Chung, B. H. Y., Cochrane, L., Corsello, C., Crawford, E. L., Crossett, A., Cytrynbaum, C., Dawson, G., de Jonge, M., Delorme, R., Drmic, I., Duketis, E., Duque, F., Estes, A., Farrar, P., Fernandez, B. A., Folstein, S. E., Fombonne, E., Freitag, C. M., Gilbert, J., Gillberg, C., Glessner, J. T., Goldberg, J., Green, A., Green, J., Guter, S. J., Hakonarson, H., Heron, E. A., Hill, M., Holt, R., Howe, J. L., Hughes, G., Hus, V., Igliozzi, R., Kim, C., Klauck, S. M., Kolevzon, A., Korvatska, O., Kustanovich, V., Lajonchere, C. M., Lamb, J. A., Laskawiec, M., Leboyer, M., le Couteur, A., Leventhal, B. L., Lionel, A. C., Liu, X. Q., Lord, C., Lotspeich, L., Lund, S. C., Maestrini, E., Mahoney, W., Mantoulan, C., Marshall, C. R., McConachie, H., McDougle, C. J., McGrath, J., McMahon, W. M., Merikangas, A., Migita, O., Minshew, N. J., Mirza, G. K., Munson, J., Nelson, S. F., Noakes, C., Noor, A., Nygren, G., Oliveira, G., Papanikolaou, K., Parr, J. R., Parrini, B., Paton, T., Pickles, A., Pilorge, M., Piven, J., Ponting, C. P., Posey, D. J., Poustka, A., Poustka, F., Prasad, A., Ragoussis, J., Renshaw, K., Rickaby, J., Roberts, W., Roeder, K., Roge, B., Rutter, M. L., Bierut, L. J., Rice, J. P., Salt, J., Sansom, K., Sato, D., Segurado, R., Sequeira, A. F., Senman, L., Shah, N., Sheffield, V. C., Soorya, L., Sousa, I., Stein, O., Sykes, N., Stoppioni, V., Strawbridge, C., Tancredi, R., Tansey, K., Thiruvahindrapduram, B., Thompson, A. P., Thomson, S., Tryfon, A., Tsiantis, J., van Engeland, H., Vincent, J. B., Volkmar, F., Wallace, S., Wang, K., Wang, Z., Wassink, T. H., Webber, C., Weksberg, R., Wing, K., Wittemeyer, K., Wood, S., Wu, J., Yaspan, B. L., Zurawiecki, D., Zwaigenbaum, L., Buxbaum, J. D., Cantor, R. M., Cook, E. H., Coon, H., Cuccaro, M. L., Devlin, B., Ennis, S., Gallagher, L., Geschwind, D. H., Gill, M., Haines, J. L., Hallmayer, J., Miller, J., Monaco, A. P., Nurnberger Jr, J. I., Paterson, A. D., Pericak-Vance, M. A., Schellenberg, G. D., Szatmari, P., Vicente, A. M., Vieland, V. J., Wijsman, E. M., Scherer, S. W., Sutcliffe, J. S., & Betancur, C. (2010). Functional impact of global rare copy number variation in autism spectrum disorders. Nature, 466(7304), 368–372.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Porter, L. M. (2001). Dietary differences among sympatric Callitrichinae in northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. labiatus. International Journal of Primatology, 22(6), 961–992.

    Article  Google Scholar 

  • Ranciaro, A., Campbell, M. C., Hirbo, J. B., Ko, W.-Y., Froment, A., Anagnostou, P., Kotze, M. J., Ibrahim, M., Nyambo, T., Omar, S. A., & Tishkoff, S. A. (2014). Genetic origins of lactase persistence and the spread of pastoralism in Africa. American Journal of Human Genetics, 94(4), 496–510.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Raubenheimer, D., Rothman, J. M., Pontzer, H., & Simpson, S. J. (2014). Macronutrient contributions of insects to the diets of hunter-gatherers: A geometric analysis. Journal of Human Evolution, 71(C), 70–76.

    Article  PubMed  Google Scholar 

  • Reese, T. A., Liang, H.-E., Tager, A. M., Luster, A. D., Van Rooijen, N., et al (2007). Chitin induces accumulation in tissue of innate immune cells associated with allergy. Nature, 447(7140), 92–96.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rose, L. M. (1994). Sex differences in diet and foraging behavior in white-faced capuchins (Cebus capucinus). International Journal of Primatology, 15(1), 95–114.

    Article  Google Scholar 

  • Rothman, J. M., Raubenheimer, D., Bryer, M. A. H., Takahashi, M., & Gilbert, C. C. (2014). Nutritional contributions of insects to primate diets: Implications for primate evolution. Journal of Human Evolution, 71(C), 59–69.

    Article  PubMed  Google Scholar 

  • Schlebusch, C. M., Sjödin, P., Skoglund, P., & Jakobsson, M. (2013). Stronger signal of recent selection for lactase persistence in Maasai than in Europeans. European Journal of Human Genetics, 21(5), 550–553.

    Article  PubMed  CAS  Google Scholar 

  • Seibold, M. A., Reese, T. A., Choudhry, S., Salam, M. T., Beckman, K., Eng, C., Atakilit, A., Meade, K., Lenoir, M., Watson, H. G., Thyne, S., Kumar, R., Weiss, K. B., Grammer, L. C., Avila, P., Schleimer, R. P., Fahy, J. V., Rodriguez-Santana, J., Rodriguez-Cintron, W., Boot, R. G., Sheppard, D., Gilliland, F. D., Locksley, R. M., & Burchard, E. G. (2009). Differential enzymatic activity of common haplotypic versions of the human acidic mammalian chitinase protein. Journal of Biological Chemistry, 284(29), 19650–19658.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of Human Evolution, 32(6), 523–559.

    Article  PubMed  CAS  Google Scholar 

  • Stankiewicz, P., & Lupski, J. R. (2010). Structural variation in the human genome and its role in disease. Annual Review of Medicine, 61, 437–455.

    Article  PubMed  CAS  Google Scholar 

  • Stone, A. I. (2007). Responses of squirrel monkeys to seasonal changes in food availability in an eastern Amazonian forest. American Journal of Primatology, 69(2), 142–157.

    Article  PubMed  Google Scholar 

  • Strait, S. G., & Vincent, J. (1998). Primate faunivores: Physical properties of prey items. International Journal of Primatology, 19(5), 867–878.

    Article  Google Scholar 

  • Strobel, S., Roswag, A., Becker, N. I., Trenczek, T. E., & Encarnação, J. A. (2013). Insectivorous bats digest chitin in the stomach using acidic mammalian chitinase. PLoS One, 8(9), e72770.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sudmant, P. H., Huddleston, J., Catacchio, C. R., Malig, M., Hillier, L. W., Baker, C., Mohajeri, K., Kondova, I., Bontrop, R. E., Persengiev, S., Antonacci, F., Ventura, M., Prado-Martinez, J., Great Ape Genome Project, Marques-Bonet, T., & Eichler, E. E. (2013). Evolution and diversity of copy number variation in the great ape lineage. Genome Research, 23(9), 1373–1382.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tabata, E., Kashimura, A., Wakita, S., Ohno, M., Sakaguchi, M., Sugahara, Y., Imamura, Y., Seki, S., Ueda, H., Matoska, V., Bauer, P. O., & Oyama, F. (2017a). Protease resistance of porcine acidic mammalian chitinase under gastrointestinal conditions implies that chitin-containing organisms can be sustainable dietary resources. Scientific Reports, 7(1), 12963.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tabata, E., Kashimura, A., Wakita, S., Ohno, M., Sakaguchi, M., Sugahara, Y., Kino, Y., Matoska, V., Bauer, P. O., & Oyama, F. (2017b). Gastric and intestinal proteases resistance of chicken acidic chitinase nominates chitin-containing organisms for alternative whole edible diets for poultry. Scientific Reports, 7(1), 6662.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tabata, E., Kashimura, A., Kikuchi, A., Masuda, H., Miyahara, R., Hiruma, Y., Wakita, S., Ohno, M., Sakaguchi, M., Sugahara, Y., Matoska, V., Bauer, P. O., & Oyama, F. (2018). Chitin digestibility is dependent on feeding behaviors, which determine acidic chitinase mRNA levels in mammalian and poultry stomachs. Scientific Reports, 8(1), 1461.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Taggart, R. T., Mohandas, T. K., Shows, T. B., & Bell, G. I. (1985). Variable numbers of pepsinogen genes are located in the centromeric region of human chromosome 11 and determine the high-frequency electrophoretic polymorphism. Proceedings of the National Academy of Sciences of the USA, 82(18), 6240–6244.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tishkoff, S. A., Reed, F. A., Ranciaro, A., Voight, B. F., Babbitt, C. C., Silverman, J. S., Powell, K., Mortensen, H. M., Hirbo, J. B., Osman, M., Ibrahim, M., Omar, S. A., Lema, G., Nyambo, T. B., Ghori, J., Bumpstead, S., Pritchard, J. K., Wray, G. A., & Deloukas, P. (2007). Convergent adaptation of human lactase persistence in Africa and Europe. Nature Genetics, 39(1), 31–40.

    Article  PubMed  CAS  Google Scholar 

  • Wang, J., Wang, H., Jiang, J., Kang, H., Feng, X., Zhang, Q., & Liu, J. F. (2013). Identification of genome-wide copy number variations among diverse pig breeds using SNP genotyping arrays. PLoS One, 8(7), e68683.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wright, P. C. (1985). The cost and benefits of nocturnality for Aotus trivirgatus (the night monkey). Ph.D. thesis, City University of New York.

  • Wright, D., Boije, H., Meadows, J. R. S., Bed’hom, B., Gourichon, D., et al (2009). Copy number variation in intron 1 of SOX5 causes the pea-comb phenotype in chickens. PLoS Genetics, 5(6), e1000512.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yoshida, K., Go, Y., Kushima, I., Toyoda, A., Fujiyama, A., et al (2016). Single-neuron and genetic correlates of autistic behavior in macaque. Science Advances, 2(9), e1600558–e1600558.

    Article  CAS  Google Scholar 

  • Zarrei, M., MacDonald, J. R., Merico, D., & Scherer, S. W. (2015). A copy number variation map of the human genome. Nature Reviews Genetics, 16(3), 172–183.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, J., Zhang, Y.-P., & Rosenberg, H. F. (2002). Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey. Nature Genetics, 30(4), 411–415.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, Z., Zheng, T., Homer, R. J., Kim, Y.-K., Chen, N. Y., Cohn, L., Hamid, Q., & Elias, J. A. (2004). Acidic mammalian chitinase in asthmatic Th2 inflammation and IL-13 pathway activation. Science, 304(5677), 1678–1682.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

I thank the editor and two anonymous reviewers for their thoughtful and constructive comments. This work was supported by funding from the Center for Human Evolutionary Studies at Rutgers University, the International Primatological Society, and a National Science Foundation DDRIG (Award #1650864). I thank Dr. P. J. Perry, Dr. Todd Disotell, and Coriell Institute (Repository numbers: NG05311, NG05313, NG06115, NG07101, NG07107, NG07921) for providing samples. Drs. Rob Scott, Erin Vogel, and Ryne Palombit provided helpful feedback on earlier versions of this article.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mareike C. Janiak.

Additional information

Handling Editor: Joanna M. Setchell

Electronic supplementary material

ESM 1

(DOCX 3086 kb)

ESM 2

(XLSX 9 kb)

ESM 3

(PDF 61 kb)

ESM 4

(XLSX 14 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Janiak, M.C. No Evidence of Copy Number Variation in Acidic Mammalian Chitinase Genes (CHIA) in New World and Old World Monkeys. Int J Primatol 39, 269–284 (2018). https://doi.org/10.1007/s10764-018-0037-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-018-0037-7

Keywords