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Evolutionary Biology

, Volume 41, Issue 4, pp 595–605 | Cite as

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

  • Daniel W. Sorensen
  • Claire Butkus
  • Lisa Noelle Cooper
  • Chris J. Cretekos
  • John J. RasweilerIV
  • Karen E. SearsEmail author
Research Article

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.

Keywords

Morphometrics Craniofacial Evolution Modularity Integration Phyllostomid Pteropodid 

Notes

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.

References

  1. Adams, D. C. (2014). Quantifying and comparing phylogenetic evolutionary rates for shape and other high-dimensional phenotypic data. Systematic Biology, 63, 166–177.PubMedCrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  4. 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.PubMedCrossRefGoogle Scholar
  5. Bennett, V., & Goswami, A. (2011). Does developmental strategy drive limb integration in marsupials and monotremes? Mammalian Biology, 76, 79–83.Google Scholar
  6. Bennett, C. V., & Goswami, A. (2013). Statistical support for the hypothesis of developmental constraint in marsupial skull evolution. BMC Biology, 11, 52.PubMedCentralPubMedCrossRefGoogle Scholar
  7. Cheverud, J. M., Wagner, G. P., & Dow, M. M. (1989). Methods for the comparative analysis of variation patterns. Systematic Zoology, 38, 201–213.CrossRefGoogle Scholar
  8. Dryden, I. L., & Mardia, K. V. (1998). Statistical shape analysis. Chichester: Wiley.Google Scholar
  9. Dumont, E. R. (1997). Cranial shape in fruit, nectar and exudate feeders. American Journal of Physical Anthropology, 102, 187–202.PubMedCrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. Dumont, E. R. (2004). Patterns of diversity in cranial shape among plant-visiting bats. Acta Chiropterologica, 6, 59–74.CrossRefGoogle Scholar
  12. 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
  13. Dumont, E. R. (2007). Feeding mechanisms in bats: Variation within the constraints of flight. Integrative and Comparative Biology, 47, 137–146.PubMedCrossRefGoogle Scholar
  14. 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.PubMedCentralCrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. Escoufier, Y. (1973). Le traitement des variables vectorielles. Biometrics, 29, 751–760.CrossRefGoogle Scholar
  17. 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
  18. 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).Google Scholar
  19. 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
  20. 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.PubMedCrossRefGoogle Scholar
  21. Gómez-Robles, A., & Polly, P. D. (2012). Morphological integration in the hominin dentition: Evolutionary, developmental, and functional factors. Evolution, 66, 1024–1043.PubMedCrossRefGoogle Scholar
  22. Goswami, A. (2006). Cranial modularity shifts during mammalian evolution. American Naturalist, 168, 270–280.PubMedCrossRefGoogle Scholar
  23. Goswami, A., & Polly, P. D. (2010). The influence of modularity on cranial morphological disparity in carnivora and primates (mammalia). PLoS One, 5, e9517.PubMedCentralPubMedCrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. Hansen, T. F., & Houle, D. (2008). Measuring and comparing evolvability and constraint in multivariate characters. Journal of Evolutionary Biology, 21, 1201–1219.PubMedCrossRefGoogle Scholar
  27. Hunt, G. (2007). Evolutionary divergence in directions of high phenotypic variance in the ostracode genus Poseidonamicus. Evolution, 61, 1560–1576.PubMedCrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. Jones, K. E., Bininda-Emonds, O. R., & Gittleman, J. L. (2005). Bats, clocks, and rocks: diversification patterns in Chiroptera. Evolution, 59, 2243–2255.PubMedCrossRefGoogle Scholar
  30. 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.PubMedCrossRefGoogle Scholar
  31. Kavanagh, K. D., Evans, A. R., & Jernvall, J. (2007). Predicting evolutionary patterns of mammalian teeth from development. Nature, 449, 427–432.PubMedCrossRefGoogle Scholar
  32. 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.CrossRefGoogle Scholar
  33. 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
  34. 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
  35. 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
  36. Klingenberg, C. P. (2005). Developmental constraints, modules and evolvability. In B. Hallgrímsson & B. K. Hall (Eds.), Variation (pp. 219–247). San Diego: Academic Press.CrossRefGoogle Scholar
  37. Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual review of ecology, evolution, and systematics, 39, 115–132.CrossRefGoogle Scholar
  38. Klingenberg, C. P. (2009). Morphometric integration and modularity in configurations of landmarks: Tools for evaluating a priori hypotheses. Evolution & Development, 11, 405–421.CrossRefGoogle Scholar
  39. Klingenberg, C. P. (2011). MorphoJ: An integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.PubMedCrossRefGoogle Scholar
  40. Klingenberg, C. P., Barluenga, M., & Meyer, A. (2002). Shape analysis of symmetric structures: Quantifying variation among individuals and asymmetry. Evolution, 56, 1909–1920.PubMedCrossRefGoogle Scholar
  41. Klingenberg, C. P., & Gidaszewski, N. A. (2010). Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Systematic Biology, 59, 245–261.PubMedCrossRefGoogle Scholar
  42. Klingenberg, C. P., & McIntyre, G. S. (1998). Geometric morphometrics of developmental instability: Analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution, 52, 1363–1375.CrossRefGoogle Scholar
  43. 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
  44. 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.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. McAdams, H. H., & Arkin, A. (1999). It’s a noisy business! genetic regulation at the nanomolar scale. Trends in Genetics, 15, 65–69.PubMedCrossRefGoogle Scholar
  47. Moller, A. P., & Swaddle, J. P. (1997). Asymmetry, developmental stability, and evolution. Oxford: Oxford University Press.Google Scholar
  48. Myers, P., Espinoza, R., Parr, S., Jones,T., Hammond,G. S., Dewey, T. A., (2013) The Animal Diversity Web (online). http://animaldiversity.org.
  49. Palmer, A. R., & Strobeck, C. (1986). Fluctuating asymmetry: Measurement, analysis, patterns. Annual Review of Ecology and Systematics, 17, 391–421.CrossRefGoogle Scholar
  50. 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.PubMedCrossRefGoogle Scholar
  51. Pavlicev, M., Cheverud, J., & Wagner, G. (2009). Measuring morphological integration using eigenvalue variance. Evolutionary Biology, 36, 157–170.CrossRefGoogle Scholar
  52. Polly, P. D. (2005). Development and phenotypic correlations: The evolution of tooth shape in Sorex araneus. Evolution & Development, 7, 29–41.CrossRefGoogle Scholar
  53. 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.CrossRefGoogle Scholar
  54. Raff, R. A. (1996). The shape of life: genes, development, and the evolution of animal form. Chicago: University of Chicago Press.Google Scholar
  55. Salazar-Ciudad, I., & Jernvall, J. (2010). A computational model of teeth and the developmental origins of morphological variation. Nature, 464, 583–586.PubMedCrossRefGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. 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.PubMedCrossRefGoogle Scholar
  58. Sears, K. E. (2004). Constraints on the morphological evolution of marsupial shoulder girdles. Evolution, 58, 2353–2370.PubMedGoogle Scholar
  59. 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
  60. 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.CrossRefGoogle Scholar
  61. 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
  62. 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.CrossRefGoogle Scholar
  63. 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.PubMedCrossRefGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. 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.CrossRefGoogle Scholar
  66. Wagner, G. (1990). A comparative study of morphological integration in Apis mellifera (insecta, hymenoptera). Journal of Zoological Systematics and Evolutionary Research, 28, 48–61.CrossRefGoogle Scholar
  67. Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36, 36–43.Google Scholar
  68. 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.PubMedCrossRefGoogle Scholar
  69. Young, N. M. (2006). Function, ontogeny and canalization of shape variance in the primate scapula. Journal of Anatomy, 209, 623–636.PubMedCentralPubMedCrossRefGoogle Scholar
  70. 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.PubMedCentralPubMedCrossRefGoogle Scholar
  71. 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.CrossRefGoogle Scholar
  72. 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

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Daniel W. Sorensen
    • 1
  • Claire Butkus
    • 1
  • Lisa Noelle Cooper
    • 2
  • Chris J. Cretekos
    • 3
  • John J. RasweilerIV
    • 4
  • Karen E. Sears
    • 1
    • 5
    Email author
  1. 1.Department of Animal Biology, School of Integrative BiologyUniversity of IllinoisUrbanaUSA
  2. 2.Department of Anatomy and NeurobiologyNortheast Ohio Medical UniversityRootstownUSA
  3. 3.Department of Biological SciencesIdaho State UniversityPocatelloUSA
  4. 4.Department of Obstetrics and GynecologyState University of Downstate Medical CenterBrooklynUSA
  5. 5.Institute for Genomic BiologyUniversity of IllinoisUrbanaUSA

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