Skip to main content

Advertisement

SpringerLink
Log in

GeMBiD, a Geometric Morphometric Approach to the Study of Biological Diversity: An Example Study of the Red Colobus (Procolobus [Piliocolobus]) Species Complex

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

Determining conservation priorities requires an understanding of biological diversity in terms of both genetic variation and phenotypic difference. The phenotype is where many adaptations are expressed and thus provides the potential for future evolution, including responses to rapidly changing environments. We suggest that applying geometric morphometrics (a set of methods related to image analysis) to the study of morphological differences among closely related populations can effectively quantify phenotypic variation in poorly studied taxa, and provide an informative estimate of the degree of morphological divergence relative to their better known relatives. The approach is simple and flexible, but has proven to be powerful. As an example of a Geometric Morphometric approach to the study of Biological Diversity (GeMBiD), we provide a preliminary estimate of the morphological distinctiveness of a poorly studied red colobus monkey, the Semliki red colobus (Procolobus sp. ellioti), by using cross-validated discriminant analyses on cranial shape data and comparing chance-corrected classification accuracy in this population with that of other populations of monkeys within and outside the red colobus lineage. By fruitfully exploiting available museum collections and by developing networks of scientists who can provide information on and study material from rare populations, GeMBiD could become a useful tool for complementing genetic analyses of biodiversity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adams, D. C., Rohlf, F. J., & Slice, D. E. (2004). Geometric morphometrics: ten years of progress following the ‘revolution. Italian Journal of Zoology, 71, 5–16.

    Article  Google Scholar 

  • Borenstein, E., Meilijson, I., & Ruppin, E. (2006). The effect of phenotypic plasticity on evolution in multipeaked fitness landscapes. Journal of Evolutionary Biology, 19, 1555–1570.

    Article  PubMed  CAS  Google Scholar 

  • Cardini, A. (2003). The geometry of marmot (Rodentia: Sciuridae) mandible: phylogeny and patterns of morphological evolution. Systematic Biology, 52, 186–205.

    Article  PubMed  Google Scholar 

  • Cardini, A., & Elton, S. (2008). Variation in guenon skulls I: species divergence, ecological and genetic differences. Journal of Human Evolution, 54, 615–637.

    Article  PubMed  Google Scholar 

  • Cardini, A., & Elton, S. (2009a). The radiation of red colobus monkeys (Primates, Colobinae): morphological evolution in a clade of endangered African primates. Zoological Journal of the Linnean Society, 157, 197–224.

    Article  Google Scholar 

  • Cardini, A., & Elton, S. (2009b). Geographic and taxonomic influences on cranial variation in red colobus monkeys (Primates, Colobinae): introducing a new approach to “morph” monkeys. Global Ecology and Biogeography, 18, 248–263.

    Article  Google Scholar 

  • Cardini, A., Thorington, R. W., Jr., & Polly, P. D. (2007). 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.

    Article  PubMed  CAS  Google Scholar 

  • Cardini, A., Diniz Filho, J. A. F., Polly, P. D., & Elton, S. (2010). Biogeographic analysis using geometric morphometrics: clines in skull size and shape in a widespread African arboreal monkey. A. M. T. Elewa (Ed.), Morphometrics for Nonmorphometricians, Lecture Notes in Earth Sciences, 124, Springer-Verlag Publishers, Heidelberg, Germany. doi:10.1007/978-3-540-95853-6_8.

  • Cardini, A., Nagorsen, D., O’Higgins, P., Polly, P. D., Thorington, R. W., Jr., & Tongiorgi, P. (2009). Detecting biological uniqueness using geometric morphometrics: an example case from the Vancouver Island marmot. Ecology, Ethology and Evolution. doi:10.1111/j.1439-0469.2008.00503.x.

    Google Scholar 

  • Colyn, MM. (1991). L’importance zoogeographique du Bassin du Fleuve Zaire pour la speciation: le cas des Primates simiens. Annales de le Musée Royal de l’Afrique Centrale, Tervuren, Sciences Zoologiques, 264, 1–250.

  • Cowlishaw, G., & Dunbar, R. I. M. (2000). Primate conservation biology. Chicago: Chicago University Press.

    Google Scholar 

  • Crandall, K. A., Bininda-Emonds, O. R. P., Mace, G. M., & Wayne, R. K. (2000). Considering evolutionary processes in conservation biology. Trends in Ecology and Evolution, 15, 290–295.

    Article  PubMed  Google Scholar 

  • DeSalle, R., Egan, M. G., & Siddall, M. (2005). The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society of London B–Biological Sciences, 360, 1905–1916.

    Article  CAS  Google Scholar 

  • Elias, M., Hill, R. I., Willmott, K. R., Dasmahapatra, K. K., Brower, A. V. Z., Mallet, J., & Jiggins, C. D. (2007). Limited performance of DNA barcoding in a diverse community of tropical butterflies. Proceedings of the Royal Society of London B–Biological Sciences, 274, 2881–2889.

    Article  CAS  Google Scholar 

  • Elton, S., Dunn, J., & Cardini, A. (2010). Size variation facilitates population divergence but does not explain it all: an example study from a widespread African monkey. Biological Journal of the Linnean Society, 101, 823–843.

    Google Scholar 

  • Fedigan, L., & Fedigan, L. M. (1988). Cercopithecus aethiops: A review of field studies. In A. Gautier-Hion, F. Bourliere, J.-P. Gautier, & J. Kingdon (Eds.), A primate radiation. Evolutionary biology of the African guenons. Cambridge: Cambridge University Press.

    Google Scholar 

  • Foote, M. (1997). The evolution of morphological diversity. Annual Review of Ecology and Systematics, 28, 129–152.

    Article  Google Scholar 

  • Groves, C. P. (2005). Order Primates. In D. E. Wilson & D. M. Reeder (Eds.), Mammal species of the world (pp. 111–184). Baltimore: The Johns Hopkins University Press.

    Google Scholar 

  • Grubb, P., Butynski, T. M., Oates, J. F., Bearder, S. K., Disotell, T. R., Groves, C. P., et al. (2003). Assessment of the diversity of African primates. International Journal of Primatology, 24, 1301–1357.

    Article  Google Scholar 

  • Hoffmann, R. S., Koeppl, J. W., & Nadler, C. F. (1979). The relationship of the amphiberigian marmots (Mammalia, Sciuridae). Occasional Papers of the Museum of Natural History of the University of Kansas, 83, 1–56.

    Google Scholar 

  • Isaac, N. J. B., Mallet, J., & Mace, G. M. (2004). Taxonomic inflation: Its influence on macroecology and conservation. Trends in Ecology and Evolution, 19, 464–469.

    Article  PubMed  Google Scholar 

  • IUCN (2010). IUCN Red List of Threatened Species. Version 2010.2. <www.iucnredlist.org> (Accessed July 1, 2010).

  • Mace, G. M. (2004). The role of taxonomy in species conservation. Philosophical Transactions of the Royal Society of London B–Biological Sciences, 359, 711–719.

    Article  Google Scholar 

  • Mace, G. M., & Purvis, A. (2008). Evolutionary biology and practical conservation: bridging a widening gap. Molecular Ecology, 17, 9–19.

    Article  PubMed  Google Scholar 

  • McGarigal, K., Cushman, S., & Stafford, S. (2000). Multivariate statistics for wildlife and ecology research. New York: Springer Verlag.

    Google Scholar 

  • Millien, V. (2006). Morphological evolution is accelerated among island mammals. PLoS Biology, 4, 1863–1868.

    CAS  Google Scholar 

  • Moritz, C., & Cicero, C. (2004). DNA barcoding: promise and pitfalls. PLoS Biology, 2, 1529–1531.

    Article  CAS  Google Scholar 

  • Nagorsen, D. W., & Cardini, A. (2009). Tempo and mode of evolutionary divergence in modern and Holocene Vancouver Island marmots (Marmota vancouverensis). Journal of Zoological Systematics and Evolutionary Research, 47, 258–267.

    Article  Google Scholar 

  • Nowak, K., Cardini, A., & Elton, S. (2008). Evolutionary acceleration in an endangered African primate: Speciation and divergence in the Zanzibar red colobus (Primates, Colobinae). International Journal of Primatology, 29, 1313–1339.

    Article  Google Scholar 

  • Rohlf, F. J. (2009). NTSYSpc, version 2.20L. Exeter Software, Setauket, NY.

  • Rohlf, F. J., & Marcus, L. F. (1993). A revolution in morphometrics. Trends in Ecology and Evolution, 8, 129–132.

    Article  Google Scholar 

  • Rohlf, F. J., & Slice, D. E. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59.

    Article  Google Scholar 

  • Rubinoff, D. (2006). Utility of mitochondrial DNA barcodes in species conservation. Conservation Biology, 20, 1026–1033.

    Article  PubMed  Google Scholar 

  • Sanfilippo, P., Cardini, A., Mackey, D., Hewitt, A., & Crowston, J. (2009). Optic disc morphology –rethinking shape. Progress in Retinal and Eye Research, 28, 227–248.

    Article  PubMed  Google Scholar 

  • SPSS for Windows. (2006). SPSS Inc., version 15. Chicago: SPSS Inc.

    Google Scholar 

  • Steppan, S. C., Akhverdyan, M. R., Lyapunova, E. A., Fraser, D. G., Vorontsov, N. N., Hoffmann, R. S., et al. (1999). Molecular phylogeny of the marmots (Rodentia, Sciuridae): tests of evolutionary and biogeographic hypotheses. Systematic Biology, 48, 715–734.

    Article  PubMed  CAS  Google Scholar 

  • Struhsaker, T. T. (2005). Conservation of red colobus and their habitats. International Journal of Primatology, 26, 525–538.

    Article  Google Scholar 

  • Ting, N. (2008a). Mitochondrial relationships and divergence dates of the African colobines: evidence of Miocene origins for the living colobus monkeys. Journal of Human Evolution, 55, 312–325.

    Article  PubMed  Google Scholar 

  • Ting, N. (2008b). Molecular systematics of red colobus monkeys (Procolobus [Piliocolobus]: Understanding the evolution of an endangered primate. Ph.D. dissertation. City University of New York Graduate Center.

  • Trewick, S. A. (2008). DNA Barcoding is not enough: mismatch of taxonomy and genealogy in New Zealand grasshoppers (Orthoptera: Acrididae). Cladistics, 24, 240–254.

    Article  Google Scholar 

  • Will, K. W., & Rubinoff, D. (2004). Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics, 20, 47–55.

    Article  Google Scholar 

Download references

Acknowledgments

We thank the many people who contributed directly and indirectly to this work. We thank Kate Nowak (Princeton University) for her permission to use specimens of Procolobus kirkii specimens that she collected from Zanzibar. We also thank Nelson Ting (City University of New York) and his coauthors in the study of the molecular systematics of Piliocolobus for sharing their preliminary results with us. We thank the editor, Joanna M. Setchell (Durham University), Eric Delson (City University of New York), and an anonymous referee, whose comments and suggestions substantially improved this paper. We also thank all the museum curators and collection managers who allowed us to study their specimens and who greatly helped during data collection.

This study was funded by grants from the Leverhulme Trust, Ruggles-Gates Fund for Biological Anthropology and the Royal Society.

Author information

Authors and Affiliations

  1. Dipartimento di Biologia, Universitá di Modena e Reggio Emilia, 41100, Modena, Italy

    Andrea Cardini

  2. Hull York Medical School, The University of Hull, Hull, HU6 7RX, UK

    Andrea Cardini & Sarah Elton

Authors
  1. Andrea Cardini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sarah Elton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea Cardini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cardini, A., Elton, S. GeMBiD, a Geometric Morphometric Approach to the Study of Biological Diversity: An Example Study of the Red Colobus (Procolobus [Piliocolobus]) Species Complex. Int J Primatol 32, 377–389 (2011). https://doi.org/10.1007/s10764-010-9475-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-010-9475-6

Keywords

Search

Navigation