Skip to main content

Advertisement

SpringerLink
Log in

Palate Variation and Evolution in New World Leaf-Nosed and Old World Fruit Bats (Order Chiroptera)

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

Two bat families, the leaf-nosed (Phyllostomidae) and fruit bats (Pteropodidae), have independently evolved the ability to consume plant resources. However, despite their similar ages, species richness and the strong selective pressures placed on the evolution of skull shape by plant-based foods, phyllostomids display more craniofacial diversity than pteropodids. In this study, we used morphometrics to investigate the distribution of palate variation and the evolution of palate diversity in these groups. We focused on the palate because evolutionary alterations in palate morphology are thought to underlie much feeding specialization in bats. We hypothesize that the distribution of palate variation differs in phyllostomids and pteropodids, and that the rate of palate evolution is higher in phyllostomids than pteropodids. The results suggest that the overall level of palate integration is higher in adult populations of pteropodids than phyllostomids but that the distribution of palate variation is otherwise generally conserved among phyllostomids and pteropodids. Furthermore, the results are consistent with these differences in palate integration likely having a developmental basis. The results also suggest that palate evolution has occurred significantly more rapidly in phyllostomids than pteropodids. These findings are consistent with a scenario in which the greater integration of the pteropodid palate has limited its evolvability.

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

Similar content being viewed by others

References

  • Adams, D. C. (2014). Quantifying and comparing phylogenetic evolutionary rates for shape and other high-dimensional phenotypic data. Systematic Biology, 63, 166–177.

    Article  PubMed  Google Scholar 

  • Adams, D. C., & Otárola-Castillo, E. (2013). Geomorph: An r package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution, 4, 393–399.

    Article  Google Scholar 

  • Almeida, F. C., Giannini, N. P., DeSalle, R., & Simmons, N. B. (2011). Evolutionary relationships of the old world fruit bats (chiroptera, pteropodidae): Another star phylogeny? BMC Evolutionary Biology, 11, 281.

    Article  PubMed Central  PubMed  Google Scholar 

  • Bell, E., Andres, B., & Goswami, A. (2011). Integration and dissociation of limb elements in flying vertebrates: a comparison of pterosaurs, birds and bats. Journal of Evolutionary Biology, 24, 2586–2599.

    Article  CAS  PubMed  Google Scholar 

  • Bennett, V., & Goswami, A. (2011). Does developmental strategy drive limb integration in marsupials and monotremes? Mammalian Biology, 76, 79–83.

    Google Scholar 

  • Bennett, C. V., & Goswami, A. (2013). Statistical support for the hypothesis of developmental constraint in marsupial skull evolution. BMC Biology, 11, 52.

    Article  PubMed Central  PubMed  Google Scholar 

  • Cheverud, J. M., Wagner, G. P., & Dow, M. M. (1989). Methods for the comparative analysis of variation patterns. Systematic Zoology, 38, 201–213.

    Article  Google Scholar 

  • Dryden, I. L., & Mardia, K. V. (1998). Statistical shape analysis. Chichester: Wiley.

    Google Scholar 

  • Dumont, E. R. (1997). Cranial shape in fruit, nectar and exudate feeders. American Journal of Physical Anthropology, 102, 187–202.

    Article  CAS  PubMed  Google Scholar 

  • Dumont, E. R. (1999). The effect of food hardness on feeding behaviour in frugivorous bats (phyllostomidae): An experimental study. Journal of Zoology, 248, 219–229.

    Article  Google Scholar 

  • Dumont, E. R. (2004). Patterns of diversity in cranial shape among plant-visiting bats. Acta Chiropterologica, 6, 59–74.

    Article  Google Scholar 

  • Dumont, E. R. (2006). The correlated evolution of cranial morphology and feeding behavior in New World fruit bats. In A. Zubaid, G. F. McCracken, & T. H. Kunz (Eds.), Functional and evolutionary ecology of bats (pp. 160–177). Chicago: University of Chicago Press.

    Google Scholar 

  • Dumont, E. R. (2007). Feeding mechanisms in bats: Variation within the constraints of flight. Integrative and Comparative Biology, 47, 137–146.

    Article  PubMed  Google Scholar 

  • Dumont, E. R., Davalos, L. M., Goldberg, A., Santana, S. E., Rex, K., & Voigt, C. C. (2012). Morphological innovation, diversification and invasion of a new adaptive zone. Proceedings of the Royal Society B Biological Sciences, 279, 1797–1805.

    Article  PubMed Central  Google Scholar 

  • Dumont, E. R., & O’Neil, R. (2004). Fruit hardness, feeding behavior, and resource partitioning in Old World fruit bats (family pteropodidae). Journal of Mammalogy, 85, 8–14.

    Article  Google Scholar 

  • Escoufier, Y. (1973). Le traitement des variables vectorielles. Biometrics, 29, 751–760.

    Article  Google Scholar 

  • Ferrarezzi, H., & Gimenez, E. D. A. (1996). Systematic patterns and the evolution of feeding habits in chiroptera (archonta: Mammalia). Journal of Computational Biology, 1, 75–94.

    Google Scholar 

  • Freeman, P. W., (1998) Form, function, and evolution in skulls and teeth of bats. In: T. H. Kunz, P. A. Racey (Eds). Bat Biology and Conservation. Smithsonian Institution Press (pp. 140–156).

  • Gardner, A. L. (1977). Feeding habits. In R. J. Baker, J. K. Jones, & D. C. Carter (Eds.), Biology of Bats of the New World family phyllostomidae, part 2 (pp. 293–350). Lubbock: Texas Tech Press.

    Google Scholar 

  • Gerber, S., Eble, G. J., & Neige, P. (2008). Allometric space and allometric disparity: A developmental perspective in the macroevolutionary analysis of morphological disparity. Evolution, 62, 1450–1457.

    Article  PubMed  Google Scholar 

  • Gómez-Robles, A., & Polly, P. D. (2012). Morphological integration in the hominin dentition: Evolutionary, developmental, and functional factors. Evolution, 66, 1024–1043.

    Article  PubMed  Google Scholar 

  • Goswami, A. (2006). Cranial modularity shifts during mammalian evolution. American Naturalist, 168, 270–280.

    Article  PubMed  Google Scholar 

  • Goswami, A., & Polly, P. D. (2010). The influence of modularity on cranial morphological disparity in carnivora and primates (mammalia). PLoS One, 5, e9517.

    Article  PubMed Central  PubMed  Google Scholar 

  • Goswami, A., Smaers, J., Soligo, C., & Polly, P. D. (2014). The macroevolutionary consequences of phenotypic integration: from development to deep time. Philosophical Transaction of the Royal Society B, 369, 20130254.

    Article  CAS  Google Scholar 

  • Hallgrímsson, B., Willmore, K., Dorval, C., & Cooper, D. M. (2004). Craniofacial variability and modularity in macaques and mice. Journal of Experimental Zoology Part B Molecular and Developmental Evolution, 302, 207–225.

    Article  Google Scholar 

  • Hansen, T. F., & Houle, D. (2008). Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21, 1201–1219.

    Article  CAS  PubMed  Google Scholar 

  • Hunt, G. (2007). Evolutionary divergence in directions of high phenotypic variance in the ostracode genus Poseidonamicus. Evolution, 61, 1560–1576.

    Article  PubMed  Google Scholar 

  • Irschick, D. J., Albertson, R. C., Brennan, P., Podos, J., Johnson, N. A., Patek, S., et al. (2013). Evo-devo beyond morphology: From genes to resource use. Trends in Ecology & Evolution, 28, 267–273.

    Article  Google Scholar 

  • Jones, K. E., Bininda-Emonds, O. R., & Gittleman, J. L. (2005). Bats, clocks, and rocks: diversification patterns in Chiroptera. Evolution, 59, 2243–2255.

    Article  PubMed  Google Scholar 

  • Jones, K. E., Purvis, A., MacLarnon, A., Binida-Emonds, O. R. P., & Simmons, N. B. (2002). A phylogenetic supertree of the bats (mammalia: chiroptera). Biological Reviews of the Cambridge Philosophical Society, 77, 223–259.

    Article  PubMed  Google Scholar 

  • Kavanagh, K. D., Evans, A. R., & Jernvall, J. (2007). Predicting evolutionary patterns of mammalian teeth from development. Nature, 449, 427–432.

    Article  CAS  PubMed  Google Scholar 

  • Kelly, M., & Sears, K. E. (2011). Reduced integration in marsupial limbs and the implications for mammalian evolution. Biological Journal of the Linnaean Society, 102, 22–36.

    Article  Google Scholar 

  • Klingenberg, C. P. (2003a). Developmental constraints, modules, and evolvability. In B. Hallgrímsson & B. K. Hall (Eds.), Variation: A central concept in biology (pp. 219–249). Oxford: Elsevier.

    Google Scholar 

  • Klingenberg, C. P. (2003b). Developmental instability as a research tool: Using patterns of fluctuating asymmetry to infer the developmental origins of morphological integration. In M. Polak (Ed.), Developmental instability: Causes and consequences (pp. 427–442). New York: Oxford University Pres.

    Google Scholar 

  • Klingenberg, C. P. (2003c). A developmental perspective on developmental instability: Theory, models and mechanisms. In M. Polak (Ed.), Developmental instability: Causes and consequences (pp. 14–34). New York: Oxford University Press.

    Google Scholar 

  • Klingenberg, C. P. (2005). Developmental constraints, modules and evolvability. In B. Hallgrímsson & B. K. Hall (Eds.), Variation (pp. 219–247). San Diego: Academic Press.

    Chapter  Google Scholar 

  • Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual review of ecology, evolution, and systematics, 39, 115–132.

    Article  Google Scholar 

  • Klingenberg, C. P. (2009). Morphometric integration and modularity in configurations of landmarks: Tools for evaluating a priori hypotheses. Evolution & Development, 11, 405–421.

    Article  Google Scholar 

  • Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.

    Article  PubMed  Google Scholar 

  • Klingenberg, C. P., Barluenga, M., & Meyer, A. (2002). Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry. Evolution, 56, 1909–1920.

    Article  PubMed  Google Scholar 

  • Klingenberg, C. P., & Gidaszewski, N. A. (2010). Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Systematic Biology, 59, 245–261.

    Article  CAS  PubMed  Google Scholar 

  • Klingenberg, C. P., & McIntyre, G. S. (1998). Geometric morphometrics of developmental instability: Analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution, 52, 1363–1375.

    Article  Google Scholar 

  • Marcus, L., Hingst-Zaher, E., & Zaher, H. (2000). Application of landmark morphometrics to skulls representing the orders of living mammals. The Italian Journal of Mammalogy, 1, 6–25.

    Google Scholar 

  • Marriog, G., & Cheverud, J. M. (2001). A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of New World monkeys. Evolution, 55, 2576–2600.

    Article  Google Scholar 

  • Marroig, G., Shirai, L., Porto, A., de Oliveira, F. B., & De Conto, V. (2009). The evolution of modularity in the mammalian skull II: Evolutionary consequences. Evolutionary Biology, 36, 136–148.

    Article  Google Scholar 

  • McAdams, H. H., & Arkin, A. (1999). It’s a noisy business! genetic regulation at the nanomolar scale. Trends in Genetics, 15, 65–69.

    Article  CAS  PubMed  Google Scholar 

  • Moller, A. P., & Swaddle, J. P. (1997). Asymmetry, developmental stability, and evolution. Oxford: Oxford University Press.

    Google Scholar 

  • Myers, P., Espinoza, R., Parr, S., Jones,T., Hammond,G. S., Dewey, T. A., (2013) The Animal Diversity Web (online). http://animaldiversity.org.

  • Palmer, A. R., & Strobeck, C. (1986). Fluctuating asymmetry: Measurement, analysis, patterns. Annual Review of Ecology and Systematics, 17, 391–421.

    Article  Google Scholar 

  • Parsons, K. J., Marquez, E., & Albertson, R. C. (2012). Constraint and opportunity: The genetic basis and evolution of modularity in the cichlid mandible. The American Naturalist, 179, 64–78.

    Article  PubMed  Google Scholar 

  • Pavlicev, M., Cheverud, J., & Wagner, G. (2009). Measuring morphological integration using eigenvalue variance. Evolutionary Biology, 36, 157–170.

    Article  Google Scholar 

  • Polly, P. D. (2005). Development and phenotypic correlations: The evolution of tooth shape in Sorex araneus. Evolution & Development, 7, 29–41.

    Article  Google Scholar 

  • Porto, A., de Oliveira, F. B., Shirai, L., De Conto, V., & Marroig, G. (2009). The evolution of modularity in the mammalian skull 1: Morphological integration patterns and magnitudes. Evolutionary Biology, 36, 118–135.

    Article  Google Scholar 

  • Raff, R. A. (1996). The shape of life: genes, development, and the evolution of animal form. Chicago: University of Chicago Press.

    Google Scholar 

  • Salazar-Ciudad, I., & Jernvall, J. (2010). A computational model of teeth and the developmental origins of morphological variation. Nature, 464, 583–586.

    Article  CAS  PubMed  Google Scholar 

  • Santana, S. E., Dumont, E. R., & Davis, J. L. (2010). Mechanics of bite force production and its relationship to diet in bats. Functional Ecology, 24, 776–784.

    Article  Google Scholar 

  • Santana, S. E., Grosse, I. R., & Dumont, E. R. (2012). Dietary hardness, loading behavior, and the evolution of skull form in bats. Evolution, 66, 2587–2598.

    Article  PubMed  Google Scholar 

  • Sears, K. E. (2004). Constraints on the morphological evolution of marsupial shoulder girdles. Evolution, 58, 2353–2370.

    PubMed  Google Scholar 

  • Sears, K. E. (2014). Differences in growth generate the diverse palate shapes of New World leaf-nosed bats (order chiroptera, family phyllostomidae). Evolutionary Biology, 41, 12–21.

    Google Scholar 

  • Sears, K. E., Goswami, A., Flynn, J. J., & Niswander, L. (2007). The correlated evolution of Runx2 tandem repeats, transcriptional activity and facial length in carnivora. Evolution & Development, 9, 555–565.

    Article  CAS  Google Scholar 

  • Simmons, N. B. (2005). Order chiroptera. In D. E. Wilson & D. M. Reeder (Eds.), Mammal species of the world: A taxonomic and geographic reference (pp. 313–529). Baltimore: Johns Hopkins University Press.

    Google Scholar 

  • Sztencel-Jabłonka, A., Jones, G., & Bogdanowicz, W. (2009). Skull morphology of two cryptic bat species: Pipistrellus pipistrellus and P. pygmaeu—A 3D geometric morphometrics approach with landmark reconstruction. Acta Chiropterologica, 11, 113–126.

    Article  Google Scholar 

  • Teeling, E. C., Springer, M. S., Madsen, O., Bates, P., O’Brien, S. J., & Murphy, W. J. (2005). A molecular phylogeny for bats illuminates biogeography and the fossil record. Science, 307, 580–584.

    Article  CAS  PubMed  Google Scholar 

  • Wagner, G. (1984). On the eigenvalue distribution of genetic and phenotypic dispersion matrices: Evidence for a non-random origin of quantitative genetic variation. Journal of Mathematical Biology, 21, 77–95.

    Article  Google Scholar 

  • Wagner, G. P. (1988). The influence of variation and developmental constraints on the rate of multivariate phenotypic evolution. Journal of Evolutionary Biology, 1, 45–66.

    Article  Google Scholar 

  • Wagner, G. (1990). A comparative study of morphological integration in Apis mellifera (insecta, hymenoptera). Journal of Zoological Systematics and Evolutionary Research, 28, 48–61.

    Article  Google Scholar 

  • Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36, 36–43.

    Google Scholar 

  • Willmore, K. E., Klingenberg, C. P., & Hallgrímsson, B. (2005). The relationship between fluctuating asymmetry and environmental variance in rhesus macaque skulls. Evolution, 59, 898–909.

    Article  PubMed  Google Scholar 

  • Young, N. M. (2006). Function, ontogeny and canalization of shape variance in the primate scapula. Journal of Anatomy, 209, 623–636.

    Article  PubMed Central  PubMed  Google Scholar 

  • Young, N. M., Wagner, G. P., & Hallgrímsson, B. (2010). Development and the evolvability of human limbs. Proceedings of the National Academy of Sciences of the United States of America, 107, 3400–3405.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zelditch, M. L., Mezey, J., Sheets, H. D., Lundrigan, B. L., & Garland, T. (2006). Developmental regulation of skull morphology II: Ontogenetic dynamics of covariance. Evolution & Development, 8, 46–60.

    Article  Google Scholar 

  • Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometrics for biologists: A primer. Boston: Elsevier Academic Press.

    Google Scholar 

Download references

Acknowledgments

We thank Bill Stanley and the staff at the Field Museum of Natural History for their generous specimen loans. We also thank the Wildlife Section, Forestry Division, Ministry of Agriculture, Land, and Marine Resources (currently in the Ministry of Public Utilities and the Environment) of the Republic of Trinidad and Tobago for the issuance of required collecting and export permits. We thank J. Marcot and B. Dumont for discussions that improved the manuscript, and L. Powers for preparation of bat skeletons. We thank A. Suarez for loan of the Canon used in this study. Finally, we thank Richard Behringer, Merla Hübler, Dan Urban and Simeon Williams for field assistance and collection of tissues in Trinidad. This work was supported by NIH NRSA F32 HD050042-01 and NSF IOS-1257873 to KS and NSF IOS-1255926 to CC.

Author information

Authors and Affiliations

  1. Department of Animal Biology, School of Integrative Biology, University of Illinois, 465 Morrill Hall, 505 South Goodwin Avenue, Urbana, IL, 61801, USA

    Daniel W. Sorensen, Claire Butkus & Karen E. Sears

  2. Department of Anatomy and Neurobiology, Northeast Ohio Medical University, 4209 State Route 44, Rootstown, OH, 44272, USA

    Lisa Noelle Cooper

  3. Department of Biological Sciences, Idaho State University, 921 South 8th Avenue, Pocatello, ID, 83209, USA

    Chris J. Cretekos

  4. Department of Obstetrics and Gynecology, State University of Downstate Medical Center, 450 Clarkson, Avenue, Brooklyn, NY, 11203, USA

    John J. Rasweiler IV

  5. Institute for Genomic Biology, University of Illinois, 1206 West Gregory Drive, Urbana, IL, 61801, USA

    Karen E. Sears

Authors
  1. Daniel W. Sorensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claire Butkus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lisa Noelle Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chris J. Cretekos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John J. Rasweiler IV
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Karen E. Sears
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karen E. Sears.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sorensen, D.W., Butkus, C., Cooper, L.N. et al. Palate Variation and Evolution in New World Leaf-Nosed and Old World Fruit Bats (Order Chiroptera). Evol Biol 41, 595–605 (2014). https://doi.org/10.1007/s11692-014-9291-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-014-9291-6

Keywords

Search

Navigation