Skip to main content

Advertisement

SpringerLink
Log in

Tracing functional adaptation in African cichlid fishes through morphometric analysis of fossil teeth: exploring the methods

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The sedimentary archive of Crater Lake Challa in East Africa contains abundant fossil teeth of cichlid fishes throughout at least the last 25,000 years. Here, we use morphometric analyses of oral teeth from the two extant Oreochromis species inhabiting Lake Challa to explore the feasibility of tracing adaptive modification of the cichlid trophic apparatus in the lake’s fossil record. We compared the performance of semi-landmark analysis (SLM) and elliptic Fourier analysis in capturing morphological variation in oral tooth crowns, and found that SLM, supplemented with tooth shaft measurements, ensured consistency with whole-body landmark analyses. Whole-body and tooth morphology data both allowed to discern between the indigenous Oreochromis hunteri and the recently introduced Oreochromis korogwe. Both species have an oral jaw arrangement of outer-row bicuspid and inner-rows tricuspid teeth, but O. hunteri has generally more slender teeth with a proportionally taller major cusp than O. korogwe, suggesting fine-scaled resource partitioning. Exploratory analysis of three fossil samples showed that the major tooth types of modern-day Oreochromis are also represented in the fossil record. Their total morphological variation is largely restricted to the morphospace occupied by contemporary teeth, suggesting a close functional relationship between ancient populations and their likely descendant, O. hunteri.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Barker, P. A., E. R. Hurrell, M. J. Leng, C. Wolff, C. Cocquyt, H. J. Sloane & D. Verschuren, 2011. Seasonality in equatorial climate over the last 25,000 years revealed by oxygen isotope records from Mount Kilimanjaro. Geology 39: 1111–1114.

    Article  CAS  Google Scholar 

  • Barluenga, M., K. N. Stölting, W. Salzburger, M. Muschick & A. Meyer, 2006. Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439: 719–723.

    Article  CAS  PubMed  Google Scholar 

  • Blaauw, M., D. Verschuren, B. van Geel, I. Kristen, B. Plessen, A. Lyaruu, D. R. Engstrom & J. van der Plicht, 2011. High-resolution 14C dating of a 25,000 year lake-sediment record from equatorial East Africa. Quaternary Science Reviews 30: 3043–3059.

    Article  Google Scholar 

  • Bookstein, F. L., 1991. Landmark methods for forms without landmarks: morphometrics of group differences in outline shape. Medical Image Analysis 1: 225–243.

    Article  Google Scholar 

  • Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Austral Ecology 18: 117–143.

    Article  Google Scholar 

  • Chessel, D., A. B. Dufour & J. Thioulouse, 2004. The ade4 package – I: one-table methods. R News 4: 5–10.

    Google Scholar 

  • Danley, P. D. & T. D. Kocher, 2001. Speciation in rapidly diverging systems: lessons from Lake Malawi. Molecular Ecology 10: 1075–1086.

    Article  CAS  PubMed  Google Scholar 

  • Dietz, E. J., 1983. Permutation tests for association between two distance matrices. Systematic Zoology 32: 21–26.

    Article  Google Scholar 

  • Elmer, K. R., T. K. Lehtonen, A. F. Kautt, C. Harrod & A. Meyer, 2010. Rapid sympatric ecological differentiation of crater lake cichlid fishes within historic times. BMC Biology 8: 60.

    Article  PubMed  PubMed Central  Google Scholar 

  • Elmer, K. R., T. K. Lehtonen, S. Fan & A. Meyer, 2013. Crater lake colonization by neotropical cichlid fishes. Evolution 67–1: 281–288.

    Article  Google Scholar 

  • Fraley, C., A. E. Raftery, T. B. Murphy & L. Scrucca, 2012. Mclust version 4 for R: normal mixture modeling for model-based clustering, classification, and density estimation. Technical Report 597, Department of Statistics, University of Washington.

  • Fryer, G., 1959. The trophic interrelationships and ecology of some littoral communities of Lake Nyasa with especial reference to the fishes, and a discussion of the evolution of a group of rock-frequenting cichlidae. Northern Rhodesia-Nyasaland Joint Fisheries Research Organization: 153–281.

  • Fryer, G. & D. T. Iles, 1972. The cichlid Fishes of the Great Lakes of Africa: Their Biology and Evolution. Oliver & Boyd, Edinburgh.

    Google Scholar 

  • Genner, M. J., G. F. Turner & S. J. Hawkins, 1999. Foraging of rocky habitat cichlid fishes in Lake Malawi: coexistence trough niche partitioning. Oecologia 121: 283–292.

    Article  Google Scholar 

  • Greenwood, P. H., 1956–1967. A revision of the Lake Victoria Haplochromis species (Pisces: Cichlidae), Part I – VIII. Bulletin of the British Museum (Natural History) – Zoology: 121–161.

  • Gunter, H. M., S. Fan, F. Xiong, P. Franchini, C. Fruciano & A. Meyer, 2013. Shaping development through mechanical strain: the transcriptional basis of diet-induced phenotypic plasticity in a cichlid fish. Molecular Ecology 22: 4516–4531.

    Article  PubMed  Google Scholar 

  • Hammer, O. Y., D. A. T. Harper & P. D. Ryan, 2001. PAST : paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 1–9.

    Google Scholar 

  • Iwata, H. & Y. Ukai, 2002. SHAPE: a computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors. Journal of Heredity 93: 384–385.

    Article  CAS  PubMed  Google Scholar 

  • Kerschbaumer, M. & C. Sturmbauer, 2011. The utility of geometric morphometrics to elucidate pathways of cichlid fish evolution. International Journal of Evolutionary Biology 290245: 1–8.

    Article  Google Scholar 

  • Koblmüller, S., K. M. Sefc & C. Sturmbauer, 2008. The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics. Hydrobiologia 615: 5–20.

    Article  Google Scholar 

  • Kruskal, J., 1964. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29: 1–27.

    Article  Google Scholar 

  • Langerhans, R. B. & T. J. DeWitt, 2004. Shared and unique features of evolutionary diversification. The American Naturalist 164: 335–349.

    Article  PubMed  Google Scholar 

  • Leinonen, T., J. M. Cano, H. Mäkinen & J. Merilä, 2006. Contrasting patterns of body shape and neutral genetic divergence in marine and lake populations of threespine sticklebacks. Journal of Evolutionary Biology 19: 1803–1812.

    Article  CAS  PubMed  Google Scholar 

  • Meyer, A., 1987. Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41: 1357–1369.

    Article  Google Scholar 

  • Moernaut, J., D. Verschuren, F. Charlet, I. Kristen, M. Fagot & M. De Batist, 2010. The seismic-stratigraphic record of lake-level fluctuations in Lake Challa: hydrological stability and change in equatorial East Africa over the last 140 kyr. Earth and Planetary Science Letters 290: 214–223.

    Article  CAS  Google Scholar 

  • Muschick, M., A. Indermaur & W. Salzburger, 2012. Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology 22: 2362–2368.

    Article  CAS  PubMed  Google Scholar 

  • Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens & H. Wagner, 2013. Vegan: community ecology package. R, package version 2.0-10.

  • Park, L. E. & A. S. Cohen, 2011. Paleoecological response of ostracods to early Late Pleistocene lake-level changes in Lake Malawi, East Africa. Palaeogeography, Palaeoclimatology, Palaeoecology 303: 71–80.

    Article  Google Scholar 

  • Perez, S. I., V. Bernal & P. N. Gonzalez, 2006. Differences between sliding semi-landmark methods in geometric morphometrics, with an application to human craniofacial and dental variation. Journal of Anatomy 208: 769–784.

    Article  PubMed  Google Scholar 

  • Core Team, R., 2014. R: A Language and Environment for Statistical Computing. Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Reinthal, P. N., 1990. The feeding habits of a group of herbivorous rock-dwelling cichlid fishes (Cichlidae: Perciformes) from Lake Malawi, Africa. Environmental Biology of Fishes 27: 215–233.

    Article  Google Scholar 

  • Reinthal, P. N., A. S. Cohen & D. L. Dettman, 2011. Fish fossils as paleo-indicators of ichthyofauna composition and climatic change in Lake Malawi, Africa. Palaeogeography, Palaeoclimatology, Palaeoecology 303: 126–132.

    Article  Google Scholar 

  • Rohlf, F. J., 2007a. TpsRelw: Thin Plate Spline Relative Warp (version 1.53). Stony Brook University, New York.

  • Rohlf, F. J., 2007b. TpsRegr: Thin Plate Spline Regress (version 1.40). Stony Brook University, New York.

  • Rohlf, F. J., 2010a. TpsUtil: Thin Plate Spline Utility (version 1.53). Stony Brook University, New York.

  • Rohlf, F. J., 2010b. TpsDig2: Thin Plate Spline Digitize (version 2.16). Stony Brook University, New York.

  • Rüber, L. & D. C. Adams, 2001. Evolutionary convergence of body shape and trophic morphology in cichlids from Lake Tanganyika. Journal of Evolutionary Biology 14: 325–332.

    Article  Google Scholar 

  • Salzburger, W., 2009. The interaction of sexually and naturally selected traits in the adaptive radiation of cichlid fishes. Molecular Ecology 18: 169–185.

    Article  PubMed  Google Scholar 

  • Salzburger, W., B. Van Bocxlaer & A. S. Cohen, 2014. Ecology and evolution of the African Great Lakes and their faunas. Annual Reviews of Ecology, Evolution and Systematics 45: 519–545.

    Article  Google Scholar 

  • Sato, A., N. Takezaki, H. Tichy, F. Figueroa, W. E. Mayer & J. Klein, 2003. Origin and speciation of haplochromine fishes in East African crater lakes investigated by the analysis of their mtDNA, mhc genes and SINEs. Molecular Biology and Evolution 20: 1448–1862.

    Article  CAS  PubMed  Google Scholar 

  • Schluter, D., 2000. The Ecology of Adaptive Radiation. Oxford University Press, New York.

    Google Scholar 

  • Seegers, L., L. De Vos & D. O. Okeyo, 2003. Annotated checklist of the freshwater fishes of Kenya. Journal of East African Natural History 92: 11–47.

    Article  Google Scholar 

  • Sheets, H. D., 2008. IMP: Integrated Morphometrics Package. Department of Physics, Canisius College, Buffalo.

    Google Scholar 

  • Sinninghe Damsté, J. S., J. Ossebaar, S. Schouten & D. Verschuren, 2012. Distribution of tetraether lipids in the 25-ka sedimentary record of Lake Challa: extracting reliable TEX86 and MBT/CBT palaeotemperatures from an equatorial African lake. Quaternary Science Reviews 50: 43–54.

    Article  Google Scholar 

  • Trewavas, E., 1983. Tilapiine Fishes of the Genera Sarotherodon, Oreochromis and Danakilia. British Museum of Natural History, London.

    Google Scholar 

  • Van Bocxlaer, B. & R. Schultheiß, 2010. Comparison of morphometric techniques for shapes with few homologous landmarks based on machine-learning approaches to biological discrimination. Paleobiology 36: 497–515.

    Article  Google Scholar 

  • Van Bocxlaer, B. & G. Hunt, 2013. Morphological stasis in an ongoing gastropod radiation from Lake Malawi. PNAS 110: 13892–13897.

    Article  PubMed  PubMed Central  Google Scholar 

  • van Rijssel, J. C., E. S. Hoogwater, M. A. Kishe-Machumu, E. van Reenen, K. V. Spits, R. C. van der Stelt, J. H. Wanink & F. Witte, 2015. Fast adaptive responses in the oral jaw of Lake Victoria cichlids. Evolution 69: 179–189.

    Article  PubMed  Google Scholar 

  • Venables, W. N. & B. D. Ripley, 2002. Modern Applied Statistics with S, 4th ed. Springer, New York.

    Book  Google Scholar 

  • Verschuren, D., J. S. S. Damsté, J. Moernaut, I. Kristen, M. Blaauw, M. Fagot, G. H. Haug & Challacea project members, 2009. Half-precessional dynamics of monsoon rainfall near the East African Equator. Nature 426: 637–641.

    Article  Google Scholar 

  • Wagner, C. E., L. J. Harmon & O. Seehausen, 2012. Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487: 366–369.

    Article  CAS  PubMed  Google Scholar 

  • Wautier, K., A. Huysseune & E. Verheyen, 2002. Tooth shape differences analyzed by biometric and morphometric approaches: a case study on two morphologically very similar lacustrine cichlid species. Connective Tissue Research 43: 103–108.

    Article  CAS  PubMed  Google Scholar 

  • Witte, F. & M. J. P. van Oijen, 1990. Taxonomy, ecology and fishery of Lake Victoria haplochromine trophic groups. Zoologische Verhandelingen 262: 1–47.

    Google Scholar 

  • Yamaoka, K., 1983. Feeding behaviour and dental morphology of algae scraping cichlids (Pisces: Teleostei) in Lake Tanganyika. African Study Monographs 4: 77–89.

    Google Scholar 

Download references

Acknowledgments

We thank Caxton Oluseno and the fishermen of Lake Challa for field assistance, Jos Snoeks for taxonomic information and Tom Geerinckx and Philippe Munyandamutsa for help with jaw and teeth preparation protocols. Moritz Muschick and an anonymous referee provided many useful suggestions that substantially improved the paper. The lake-sediment cores used in this study were collected under permit 13/001/11C of the Kenyan Ministry of Education, Science and Technology, in the framework of the European Science Foundation’s EuroCLIMATE project CHALLACEA. This work is financed by the CRA program of the Ghent University Research Council to D.V., and by postdoctoral fellowships of the Smithsonian Institution, the Alexander von Humboldt Foundation and the Flanders Research Foundation to B. V. B.

Author information

Author notes

  1. Claudia Manntschke

    Present address: Institute of Earth and Environmental Science, Universität Potsdam, Karl-Liebknecht-Str. 24-25, 14476, Potsdam, Germany

Authors and Affiliations

  1. Limnology Unit, Department of Biology, Ghent University, K. L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Jorunn Dieleman, Bert Van Bocxlaer, Claudia Manntschke & Dirk Verschuren

  2. Departments of Paleobiology and Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, 20013, USA

    Bert Van Bocxlaer

  3. Department of Animal Ecology and Systematics, Justus Liebig Universität, Heinrich-Buff-Ring 26-32 IFZ, 35392, Giessen, Germany

    Bert Van Bocxlaer

  4. Ichthyology Section, Zoology Department, National Museums of Kenya, P.O. Box 40658-00100, Nairobi, Kenya

    Dorothy Wanja Nyingi

  5. Evolutionary Morphology of Vertebrates, Department of Biology, Ghent University, K. L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Dominique Adriaens

Authors
  1. Jorunn Dieleman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bert Van Bocxlaer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claudia Manntschke
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dorothy Wanja Nyingi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dominique Adriaens
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dirk Verschuren
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jorunn Dieleman.

Additional information

Handling editor: M. Power

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dieleman, J., Van Bocxlaer, B., Manntschke, C. et al. Tracing functional adaptation in African cichlid fishes through morphometric analysis of fossil teeth: exploring the methods. Hydrobiologia 755, 73–88 (2015). https://doi.org/10.1007/s10750-015-2218-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-015-2218-0

Keywords

Search

Navigation