Evolutionary Acceleration and Divergence in Procolobus kirkii

  • Katarzyna NowakEmail author
  • Andrea Cardini
  • Sarah Elton


We investigated the role of geographical insularity in divergence and speciation of Procolobus kirkii by examining cranial morphology. The sample (n = 369) included museum specimens of Procolobus spp. and recently deceased individuals of P. kirkii from the main island of Zanzibar and 2 smaller islands in the archipelago. Geometric morphometrics evinced pronounced divergence of Procolobus kirkii from mainland Procolobus, including members of P. badius ssp., P. pennantii ssp., P. rufomitratus, P. gordonorum and also representatives of the assemblage of red colobus populations from Central Equatorial Africa. Procolobus kirkii has a small cranium, consistent with the island rule for large mammals, reduced sexual dimorphism consistent with Rensch’s rule, and a distinct cranial form. Analyses of phenotypic variance of Procolobus kirkii gave no evidence for population bottlenecks in the history of the species, but there is a clear indication that the species has experienced accelerated morphological evolution of size, probably as a result of insularity. Their highly distinctive morphology lends weight to the argument that they are a unique insular endemic species in need of active conservation.


endemism geometric morphometrics island rule Procolobus taxonomy 



We dedicate this paper to the memory of Marco Corti (1950–2007) in recognition of his great contribution to the development and application of geometric morphometrics to the study of systematics and the mechanisms of speciation in mammals. An eclectic scientist, Marco may have been the first to use the term geometric morphometrics. With his studies, he was a pioneer, clearing the path and serving as an inspiration for many mammalogists. His papers were a model to follow for many of us and his advice was invaluable for many young zoologists who were struggling to learn geometric morphometrics and multivariate statistics. We are deeply grateful to all museum curators and collection managers who allowed and helped us to study their collections. Among them, we especially thank Hans-Walter Mittmann (Staatliches Museum für Naturkunde, Karlsruhe) for sending us specimens on loan during our visit at the Museum für Naturkunde in Berlin. Wim Wendelen (Royal Museum for Central Africa, Tervuren) and Olav Olav Röhrer-Ertl (formerly at Staatliche Naturwissenschaftliche Sammlugen Bayerns, Munich) provided invaluable help with specimen identification and advice on collections of Procolobus, and Cristina Murari (University of Modena and Reggio Emilia) provided crucial support for running computer analyses on Linux work stations. Claudio Gentilini, Maria Teresa Martinelli, Roberta Cantaroni, Costantino Crescimanno and Andrea Ghidoni (all of them at the University of Modena and Reggio Emilia) also were of great help to solving computer and network problems. For their support of our study, we sincerely thank Robert J. Asher and the University Museum of Zoology in Cambridge, where the specimens of Procolobus kirkii collected by K. Nowak are held. Craig Ludwig (National Museum of Natural History, Washington), Emiliano Bruner and Paolo Colangelo (University of Rome), Damiano Preatoni and Adriano Martinoli (University of Insubria), and Andrew Marshall (University of York) were of great help during various stages of this study. We also thank Zanzibar authorities in the Department of Commercial Crops, Fruits and Forestry (DCCFF), especially Director Dr. Bakari Asseid, for logistical support in situ. We particularly thank a reviewer of one of our previous papers for their advice on and suggestions about how to recalculate the partial disparity analysis so that the clumped means did not overly influence the analysis. Finally, we thank Nelson Ting (City University of New York) and his coauthors for sharing with us the preliminary results of their study of the molecular systematics of Piliocolobus, and Colin Groves (Australian National University) for his always invaluable advice on primate taxonomy and his careful review which improved a previous version of this manuscript. Grants from the Leverhulme Trust and the Ruggles-Gates Fund for Biological Anthropology provided funding for the study.


  1. Adams, D. C., Slice, D. E., & Rohlf, F. J. (2004). Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71, 5–16.CrossRefGoogle Scholar
  2. Bookstein, F. L. (1991). Morphometric Tools for Landmark Data. Cambridge,UK: Cambridge University Press.Google Scholar
  3. Bromham, L., & Cardillo, M. (2007). Primates follow the ‘island rule’: Implications for interpreting Homo floresiensis. Biology Letters, 3, 398–400.PubMedCrossRefGoogle Scholar
  4. Brown, P., Sutikna, T., Morwood, M. J., Soejono, R. P., Jatmiko, A., Wayhu Saptomo, E., & Awedue, R. (2004). A new small-bodied hominin from the Late Pleistocene of Flores, Indonesia. Nature, 431, 1055–1061.PubMedCrossRefGoogle Scholar
  5. Burgess, N. D., Clarke, G. P., & Rodgers, W. A. (1998). Coastal forests of eastern Africa: Status, endemism patterns and their potential causes. Biological Journal of the Linnaean Society of London, 64, 337–367.CrossRefGoogle Scholar
  6. Camperio Ciani, A., Palentini, L., & Finotto, E. (2001). Survival of a small translocated Procolobus kirkii population on Pemba Island. Biodiversity and Conservation, 24, 15–18.Google Scholar
  7. Cardini, A., & Elton, S. (2007). Sample size and sampling error in geometric morphometric studies of size and shape. Zoomorphology, 126, 121–134.CrossRefGoogle Scholar
  8. Cardini, A., & Elton, S. (2008a). Does the skull carry a phylogenetic signal? Evolution and modularity in the guenons. Biological Journal of the Linnean Society of London, 93, 813–834.CrossRefGoogle Scholar
  9. Cardini, A., & Elton, S. (2008b). Variation in guenon skulls I: species divergence, ecological and genetic differences. Journal of Human Evolution, 54, 615–637.PubMedCrossRefGoogle Scholar
  10. Cardini, A., & Elton, S. (2008c). Variation in guenon skulls II: sexual dimorphism. Journal of Human Evolution, 54, 638–647.PubMedCrossRefGoogle Scholar
  11. Cardini, A., & O’Higgins, P. (2004). Patterns of morphological evolution in Marmota (Rodentia, Sciuridae): Geometric morphometrics of the cranium in the context of marmot phylogeny, ecology and conservation. Biological Journal of the Linnaean Society, 82(3), 385–407.CrossRefGoogle Scholar
  12. Cardini, A., & Thorington Jr., R. W. (2006). Post-natal ontogeny of the marmot (Rodentia, Sciuridae) cranium: Allometric trajectories and species divergence. Journal of Mammalogy, 87, 201–216.CrossRefGoogle Scholar
  13. Cardini, A., Jansson, A.-U., & Elton, S. (2007a). Ecomorphology of vervet monkeys: A geometric morphometric approach to the study of clinal variation. Journal of Biogeography, 34, 1663–1678.CrossRefGoogle Scholar
  14. Cardini, A., Thorington Jr., R. W., & Polly, P. D. (2007b). Evolutionary acceleration in the most endangered mammal of Canada: Phylogenetic signal and cranial divergence in the Vancouver Island marmot (Rodentia, Sciuridae). Journal of Evolutionary Biology, 20, 1833–1846.PubMedCrossRefGoogle Scholar
  15. Carson, H. L., & Templeton, A. R. (1984). Genetic revolutions in relation to speciation phenomena: The founding of new populations. Annual Review of Ecological Systems, 15, 97–131.CrossRefGoogle Scholar
  16. Channell, R., & Lomolino, M. V. (2000). Dynamic biogeography and conservation of endangered species. Nature, 403, 84–86.PubMedCrossRefGoogle Scholar
  17. Colyn, M. M. (1991). L’importance zoog’eographique du Bassin du Fleuve Zaire pour la speciation: le cas des Primates simiens. Annalen Zoologische Wetenschappen, Koninklijk Museum Voor Midden-Afrika Tervuren, Belgie, 264, 1–250.Google Scholar
  18. Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer Associates.Google Scholar
  19. Delson, E. (1994). Evolutionary history of the colobine monkeys in paleoenvironmental perspective. In A. G. Davies, & J. F. Oates (Eds.), Colobine monkeys: Their ecology, behavior and evolution (pp. 11–43). Cambridge, UK: Cambridge University Press.Google Scholar
  20. Dryden, I. L., & Mardia, K. V. (1998). Statistical Shape Analysis. New York: John Wiley & Sons.Google Scholar
  21. Fairbairn, D. J. (1997). Allometry for sexual size dimorphism: Pattern and process in the coevolution of body size in males and females. Annual Review of Ecological Systems, 28, 659–687.CrossRefGoogle Scholar
  22. Fontaneto, D., Melone, G., & Cardini, A. (2004). Geometric morphometrics study of the jaws in microscopic aquatic pseudocoelomates: Shape diversity in the trophy of different species of Rotaria (Rotifera, Bdelloidea). Italian Journal of Zoology, 71, 63–72.Google Scholar
  23. Fooden, J., & Albrecht, G. H. (1993). Latitudinal and insular variation of skull size in crab-eating macaques (primates, Cercopithecidae: Macaca fascicularis). American Journal of Physical Anthropology, 92, 521–538.PubMedCrossRefGoogle Scholar
  24. Foster, J. B. (1964). Evolution of mammals on islands. Nature, 202, 234–235.CrossRefGoogle Scholar
  25. Galat-Luong, A., & Galat, G. (2005). Conservation and survival adaptations of Temminck’s red colobus (Procolobus badius temminckii) in Senegal. International Journal of Primatology, 26, 585–603.CrossRefGoogle Scholar
  26. Goldman, H. V., & Walsh, M. T. (1997). A leopard in jeopardy: An anthropological survey of practices and beliefs which threaten the survival of the Zanzibar leopard (Panthera pardus adersi). Unpublished report to the Department of Commercial Crops, Fruits, and Forestry, Zanzibar.Google Scholar
  27. Goltsman, M., Kruchenkova, E. P., Sergeev, S., Volodin, I., & Macdonald, D. W. (2005). “Island syndrome” in a population of Arctic foxes (Alopex lagopus) from Mednyi Island. Journal of Zoology, 267, 405–418.CrossRefGoogle Scholar
  28. Groves, C. P. (2001). Primate Taxoxomy. Washington, DC: Smithsonian Institution Press.Google Scholar
  29. Groves, C. P. (2007). The taxonomic diversity of the Colobinae of Africa. Journal of Anthropological Science, 85, 7–34.Google Scholar
  30. Grubb, P. (2006). Geospecies and superspecies in the African primate fauna. Primate Conservation, 20, 75–78.CrossRefGoogle Scholar
  31. Grubb, P., Butynski, T. M., Oates, J. F., Bearder, S. K., Disotell, T. R., Groves, C. P., & Struhsaker, T. T. (2003). Assessment of the diversity of African primates. International Journal of Primatology, 24, 1301–1357.CrossRefGoogle Scholar
  32. Helbig, A. J., Knox, A. G., Parkin, D. T., Sangster, G., & Collinson, M. (2002). Guidelines for assigning species rank. Ibis, 144, 518–525.CrossRefGoogle Scholar
  33. Hilton-Taylor, C. (2000). 2000 IUCN Red List of Threatened Species. Cambridge, UK: IUCN.Google Scholar
  34. Howell, D. C. (2002). Statistical Methods for Psychology (pp. 384–387, 5th ed.). Pacific Grove, CA: Duxbury Thompson Learning.Google Scholar
  35. IUCN (2000). 2000 IUCN Red List of Threatened Species. Cambridge, UK: IUCN.Google Scholar
  36. Kingdon, J. (1981). Where have the colonists come from? A zoogeographical examination of some mammalian isolates in eastern Africa. African Journal of Ecology, 19, 115–124.CrossRefGoogle Scholar
  37. Kingdon, J. (1990). Island Africa: The evolution of Africa’s rare animals and plants. London: William Collins Sons.Google Scholar
  38. Kingdon, J. (1997). The kingdon field guide to African mammals. Princeton: Princeton University Press.Google Scholar
  39. Klingenberg, C. P., & Monteiro, L. R. (2005). Distances and directions in multidimensional shape spaces: Implications for morphometric applications. Systems Biology, 54, 678–688.CrossRefGoogle Scholar
  40. Lomolino, M. V. (1985). Body size of mammals on islands: the island rule re-examined. American Naturalist, 125, 310–316.CrossRefGoogle Scholar
  41. Lomolino, M. V., Sax, D. F., Riddle, B. R., & Brown, J. H. (2006). The island rule and a research agenda for studying ecogeographical patterns. Journal of Biogeography, 33, 1503–1510.CrossRefGoogle Scholar
  42. Manly, B. (1997). Randomization, bootstrap, and Monte Carlo methods in biology (2nd ed.). London: Chapman and Hall.Google Scholar
  43. Marcus, L. F., Hingst-Zaher, E., & Zaher, H. (2000). Application of landmark morphometrics to skulls representing the orders of living mammals. Hystrix, 11, 27–48.Google Scholar
  44. Mayr, E. (1963). Animal Species and Evolution. Cambridge, MA: Harvard University Press.Google Scholar
  45. McFarland, M. J. (1986). Ecological determinants of fission-fusion sociality in Ateles and Pan. In J. G. Else, & P. C. Lee (Eds.), Primate ecology and conservation, Vol. 2 (pp. 181–190). Cambridge, UK: Cambridge University Press.Google Scholar
  46. Meiri, S., Cooper, N., & Purvis, A. (2008). The island rule: made to be broken? Proceedings of the Royal Society of London B – Biological Science, 275, 141–148.CrossRefGoogle Scholar
  47. Millien, V. (2006). Morphological evolution is accelerated among island mammals. PLoS Biology, 4, 1863–1868.Google Scholar
  48. Millien, V. (2007). Spurious or island effect? A response to J. A. Pérez-Claros and J. C. Aledo’s comment on Morphological evolution is accelerated among island mammals. PLoS Biology, 5(7), e176. doi: 10.1371/journal.pbio.0050176.PubMedCrossRefGoogle Scholar
  49. Mturi, F. A. (1991). The Feeding Ecology and Behavior of the Red Colobus Monkey (Colobus badius kirkii). Ph.D. dissertation, University of Dar es Salaam, Dar es Salaam, Tanzania.Google Scholar
  50. Napier, P. H. (1985). Catalogue of Primates in the British Museum (Natural History) and Elsewhere in the British Isles. Part III: Family Cercopithecidae, subfamily Colobinae. London: British Museum (Natural History).Google Scholar
  51. Nowak, K. (2008). Frequent water drinking by Zanzibar red colobus (Procolobus kirkii) in a mangrove forest refuge. American Journal of Primatology, 70, 1081–1092.PubMedCrossRefGoogle Scholar
  52. Nowak, K. (2007). Behavioral Flexibility and Demography of Procolobus kirkii across Floristic and Disturbance Gradients. Ph.D. dissertation, University of Cambridge, Cambridge, UK.Google Scholar
  53. Oates, J. F., & Davies, A. G. (1994). What are the colobines? In A. G. Davies, & J. F. Oates (Eds.), Colobine monkeys: Their ecology, behavior and evolution (pp. 1–9). Cambridge, UK: Cambridge University Press.Google Scholar
  54. O’Higgins, P., Jones, N. (2006). Tools for statistical shape analysis, Hull York Medical School.
  55. Palkovacs, E. P. (2003). Explaining adaptive shifts in body size on islands: A life history approach. Oikos, 103, 37–44.CrossRefGoogle Scholar
  56. Perez-Claros, J. A., & Aledo, J. C. (2007). Comment on “Morphological evolution is accelerated among island mammals”. PLoS Biology, 5(7), e180.PubMedCrossRefGoogle Scholar
  57. Rensch, B. (1959). Evolution above the species level. London: Methuen.Google Scholar
  58. Rodgers, W. A. (1981). The distribution and conservation status of colobus monkeys in Tanzania. Primates, 22, 33–45.CrossRefGoogle Scholar
  59. Rodgers, W. A., Owen, C. F., & Homewood, K. M. (1982). Biogeography of East African forest mammals. Journal of Biogeography, 9, 41–54.CrossRefGoogle Scholar
  60. Rohlf, F. J. (1998). On applications of geometric morphometrics to study of ontogeny and phylogeny. Systems Biology, 47, 147–158.CrossRefGoogle Scholar
  61. Rohlf, F. J. (2006a). TpsSmall. Department of Ecology and Evolution, State University of New York, Stony Brook, New York. Http:// Scholar
  62. Rohlf, F. J. (2006b). NTSYSpc, version 2.20L. Setauket, New York: Exeter Software.Google Scholar
  63. Rohlf, F. J., & Marcus, L. F. (1993). A revolution in morphometrics. Trends in Ecological Evolution, 8, 129–132.CrossRefGoogle Scholar
  64. Rohlf, F. J., & Slice, D. E. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59.CrossRefGoogle Scholar
  65. Schultz, A. H. (1957). Cranial and dental variability in colobus monkeys. Proceedings of the Zoological Society of London, 130, 79–105.Google Scholar
  66. Siex, K. S. (2003). Effects of population compression on the demography, ecology, and behavior of the Zanzibar Red Colobus Monkey (Procolobus kirkii). Ph.D. Dissertation, Duke University, Durham, NC.Google Scholar
  67. Siex, K. S., & Struhsaker, T. T. (1999). Ecology of the Zanzibar red colobus monkey: Demographic variability and habitat stability. International Journal of Primatology, 20, 163–191.CrossRefGoogle Scholar
  68. Silkiluwasha, F. (1981). The distribution and conservation status of the Zanzibar red colobus. African Journal of Ecology, 19, 187–194.CrossRefGoogle Scholar
  69. Slice, D. E. (1999). Morpheus (beta version). Stony Brook, New York: Department of Ecology and Evolution, State University of New York.Google Scholar
  70. Smith, R. J., & Cheverud, J. M. (2002). Scaling of sexual dimorphism in body mass: A phylogenetic analysis of Rensch’s rule in primates. International Journal of Primatology, 23, 1095–1135.CrossRefGoogle Scholar
  71. Struhsaker, T. T. (1975). The Red Colobus Monkey. Chicago: University of Chicago Press.Google Scholar
  72. Struhsaker, T. T. (1981). Vocalizations, phylogeny and palaeogeography of red colobus monkeys (Colobus badius). African Journal of Ecology, 19, 265–283.CrossRefGoogle Scholar
  73. Struhsaker, T. T. (2000). The effects of predation and habitat quality on the socioecology of African monkeys: Lessons from the islands of Bioko and Zanzibar. In P. F. Whitehead, & C. J. Jolly (Eds.), Old World Monkeys (pp. 393–430). Cambridge, UK: Cambridge University Press.Google Scholar
  74. Struhsaker, T. T. (2005). Conservation of red colobus and their habitats. International Journal of Primatology, 26, 525–538.CrossRefGoogle Scholar
  75. Struhsaker, T. T., & Leland, L. (1980). Observations on two rare and endangered populations of red colobus monkeys in East Africa: Colobus badius gordonorum and Colobus badius kirkii. African Journal of Ecology, 18, 191–216.CrossRefGoogle Scholar
  76. Struhsaker, T. T., & Siex, K. S. (1998). Translocation and introduction of the Zanzibar red colobus monkey: Success and failure with an endangered island endemic. Oryx, 32, 277–284.CrossRefGoogle Scholar
  77. Tappen, N. C. (1960). Problems of distribution and adaptation of the African monkeys. Current Anthropology, 1, 91–120.CrossRefGoogle Scholar
  78. Templeton, A. R. (1980). The theory of speciation via the founder principle. Genetics, 93, 1011–1038.Google Scholar
  79. Ting, N. (2008). Mitochondrial relationships and divergence dates of the African colobines: evidence of Miocene origins for the living colobus monkeys. Journal of Human Evolution, xx, 1–14.Google Scholar
  80. Ting, N., Delson, E., Oates, J. F., & Disotell, T. R. (2006). Molecular systematics of red colobus monkeys (Procolobus [Piliocolobus]). International Journal of Primatology, 27(Suppl 1), Abstract 96.Google Scholar
  81. Van Valen, L. M. (1973). Pattern and the balance of nature. Evolutionary Theory, 1, 31–49.Google Scholar
  82. Van Valen, L. M. (1978). The statistics of variation. Evolutionary Theory, 4, 33–43.Google Scholar
  83. Verheyen, W. N. (1962). Contribution a la craniologie comparee des Primates: les genres Colobus Illiger 1811 et Cercopithecus Linne 1758. Musee Royal de l’Afrique Central Tervuren, Belgique Annales Sciences Zoologiques, 105, 1–255.Google Scholar
  84. Woolfit, M., & Bromham, L. (2005). Population size and molecular evolution on islands. Proceeding of the Royal Society of Biology B, 272, 2277–2282.CrossRefGoogle Scholar
  85. Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric Morphometrics for Biologists: A Primer pp. 291–320. London: Elsevier Academic Press.Google Scholar
  86. Zuberbuehler, K., & Jenny, D. (2002). Leopard predation and primate evolution. Journal of Human Evolution, 43, 873–886.CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Wildlife Conservation Research Unit (WildCRU)University of OxfordAbingdonUK
  2. 2.Museo di Paleobiologia e dell’Orto BotanicoUniversitá di Modena e Reggio EmiliaModenaItaly
  3. 3.Hull York Medical SchoolThe University of HullHullUK

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