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5 - The influence of character correlations on phylogenetic analyses: a case study of the carnivoran cranium

Published online by Cambridge University Press:  05 July 2014

Anjali Goswami
Affiliation:
University of Cambridge
P. David Polly
Affiliation:
Indiana University
Anjali Goswami
Affiliation:
University College London
Anthony Friscia
Affiliation:
University of California, Los Angeles
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Summary

Introduction

Character independence is a major assumption in many morphology-based phylogenetic analyses (Felsenstein, 1973; Emerson and Hastings, 1998). However, the fact that most studies of modularity and morphological integration have found significant correlations among many phenotypic traits worryingly calls into question the validity of this assumption. Because gathering data on character correlations for every character in every taxon of interest is unrealistic, studies of modularity are more tractable for assessing the impact of character non-independence on phylogenetic analyses in a real system because modules summarise broad patterns of trait correlations. In this study, we use empirically derived data on cranial modularity and morphological integration in the carnivoran skull to assess the impact of trait correlations on phylogenetic analyses of Carnivora.

Carnivorans are a speciose clade of over 270 living species, with an extremely broad range of morphological and dietary diversity, from social insectivores to folivores to hypercarnivores (Nowak, 1999; Myers, 2000). This diversity offers many opportunities to isolate various potential influences on morphology, and, in this case, to study the effects of trait correlations on cranial morphology. Carnivorans also have an excellent fossil record, providing the opportunity to examine morphologies not represented in extant species, such as in the sabre-toothed cat Smilodon. Perhaps most importantly, several recent molecular and morphological studies of carnivoran phylogeny (Hunt and Tedford, 1993; Wyss and Flynn, 1993; Tedford et al., 1995; Flynn and Nedbal, 1998; Flynn et al., 2000, 2005; Flynn and Wesley-Hunt, 2005; Wesley-Hunt and Flynn, 2005; Flynn et al., this volume) provide the necessary resolution to assess the influence of character correlations on morphology-based phylogenetic analyses.

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Carnivoran Evolution
New Views on Phylogeny, Form and Function
, pp. 141 - 164
Publisher: Cambridge University Press
Print publication year: 2010

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References

Ackermann, R. R. and Cheverud, J. M. (2000). Phenotypic covariance structure in tamarins (genus Saguinus): a comparison of variation patterns using matrix correlation and common principal components analysis. American Journal of Physical Anthropology, 111, 489–501.3.0.CO;2-U>CrossRefGoogle Scholar
Ackermann, R. R. and Cheverud, J. M. (2004). Morphological integration in primate evolution. In Phenotypic Integration, ed. Pigliucci, M. and Preston, K.. Oxford: Oxford University Press, pp. 302–19.Google Scholar
Atchley, W. R. and Hall, B. K. (1991). A model for development and evolution of complex morphological structures. Biological Reviews, 66, 101–57.CrossRefGoogle ScholarPubMed
Atchley, W. R., Rutledge, J. J. and Cowley, D. E. (1982). A multivariate statistical analysis of direct and correlated response to selection in the rat. Evolution, 36, 677–98.CrossRefGoogle ScholarPubMed
Badyaev, A. V. and Foresman, K. R. (2000). Extreme environmental change and evolution: stress-induced morphological variation is strongly concordant with patterns of evolutionary divergence in shrew mandibles. Proceedings of the Royal Society of London Biological Sciences Series B, 267, 371–77.CrossRefGoogle ScholarPubMed
Badyaev, A. V. and Foresman, K. R. (2004). Evolution of morphological integration. I. Functional units channel stress-induced variation in shrew mandibles. American Naturalist, 163, 868–79.CrossRefGoogle ScholarPubMed
Bolker, J. A. (2000). Modularity in development and why it matters to evo-devo. American Zoologist, 40, 770–76.Google Scholar
Chernoff, B. and Magwene, P. M. (1999). Afterword. In Morphological Integration, ed. Olson, E. C. and Miller, R. L.. Chicago, IL: University of Chicago Press, pp. 319–48.Google Scholar
Cheverud, J. M. (1982). Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution, 36, 499–516.CrossRefGoogle ScholarPubMed
Cheverud, J. M. (1988). Spatial-analysis in morphology illustrated by rhesus macaque cranial growth and integration. American Journal of Physical Anthropology, 75, 195–96.Google Scholar
Cheverud, J. M. (1989). A comparative analysis of morphological variation patterns in the papionines. Evolution, 43, 1737–47.CrossRefGoogle Scholar
Cheverud, J. M. (1995). Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. American Naturalist, 145, 63–89.CrossRefGoogle Scholar
Cheverud, J. M. (1996a). Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins. Journal of Evolutionary Biology, 9, 5–42.CrossRefGoogle Scholar
Cheverud, J. M. (1996b). Developmental integration and the evolution of pleiotropy. American Zoologist, 36, 44–50.CrossRefGoogle Scholar
Eble, G. (2004). The macroevolution of phenotypic integration. In Phenotypic Integration, ed. Pigliucci, M. and Preston, K.. Oxford: Oxford University Press, pp. 253–73.Google Scholar
Emerson, S. B. and Hastings, P. A. (1998). Morphological correlations in evolution: Consequences for phylogenetic analysis. The Quarterly Review of Biology, 73, 141–62.CrossRefGoogle Scholar
Felsenstein, J. (1973). Maximum likelihood and minimum-steps methods for estimating evolutionary trees from data on discrete characters. Systematic Zoology, 22, 240–49.CrossRefGoogle Scholar
Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist, 125, 1–15.CrossRefGoogle Scholar
Flynn, J. J. and Nedbal, M. A. (1998). Phylogeny of the carnivora (mammalia): Congruence versus incompatability among multiple data sets. Molecular Phylogenetics and Evolution, 9, 414–26.CrossRefGoogle Scholar
Flynn, J. J. and Wesley-Hunt, G. D. (2005). Carnivora. In The Rise of Placental Mammals: Origins and Relationships of the Major Extant Clades, ed. Archibald, D. and Rose, K.. Baltimore, MD: Johns Hopkins University Press, pp. 175–98.
Flynn, J. J., Nedbal, M. A., Dragoo, J. W. and Honeycutt, R. L. (2000). Whence the red panda?Molecular Phylogenetics and Evolution, 17, 190–99.CrossRefGoogle ScholarPubMed
Flynn, J. J., Finarelli, J. A., Zehr, S., Hsu, J. and Nedbal, M. A. (2005). Molecular phylogeny of the Carnivora (Mammalia): assessing the impact of increased sampling on resolving enigmatic relationships. Systematic Biology, 54, 317–37.CrossRefGoogle ScholarPubMed
Gilbert, S. F., Opitz, J. M. and Raff, R. A. (1996). Resynthesizing evolutionary and developmental biology. Developmental Biology, 173, 357–72.CrossRefGoogle ScholarPubMed
Gonzáles-José, R., Escapa, I., Neves, W. A., Cúneo, R. and Pucciarelli, H. M. (2008). Cladistical analysis of continuous modularized traits provides phylogenetic signal in Homo evolution. Nature, 453, 775–78.CrossRefGoogle Scholar
Goswami, A. (2006a). Cranial modularity shifts during mammalian evolution. American Naturalist, 168, 270–80.CrossRefGoogle ScholarPubMed
Goswami, A. (2006b). Morphological integration in the carnivoran skull. Evolution, 60, 169–83.CrossRefGoogle ScholarPubMed
Goswami, A. (2007a). Cranial integration, phylogeny, and diet in australodelphian marsupials. PLoS One, 2, e995.CrossRefGoogle ScholarPubMed
Goswami, A. (2007b). Cranial modularity and sequence heterochrony in mammals. Evolution & Development, 9, 290–98.CrossRefGoogle ScholarPubMed
Goswami, A. and Polly, P. D. (2010). The influence of modularity on cranial morphological disparity in carnivora and primates (Mammalia). PLoS One, 5, e9517.CrossRefGoogle Scholar
Gower, J. C. (1966). Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika, 53, 325–38.CrossRefGoogle Scholar
Harris, S. R., Gower, D. J. and Wilkinson, M. (2003). Intraorganismal homology, character construction, and the phylogeny of aetosaurian archosaurs (Reptilia, Diapsida). Systematic Biology, 52, 239–52.CrossRefGoogle Scholar
Huelsenbeck, J. P. and Nielsen, R. (1999). Effect of nonindependence substitution on phylogenetic accuracy. Systematic Biology, 48, 317–28.CrossRefGoogle Scholar
Hunt, R. M. J. and Tedford, R. H. (1993). Phylogenetic relationships within aeluroid Carnivora and implications of their temporal and geographic distribution. In Mammal Phylogeny ed. Szalay, F. S., Novacek, M. J. and McKenna, M. C.. New York, NY: Springer, pp. 53–73.CrossRefGoogle Scholar
Kangas, A. T., Evans, A. R., Thesleff, I. and Jernvall, J. (2004). Non-independence of mammalian dental characters. Nature, 432, 211–14.CrossRefGoogle Scholar
Kluge, A. G. (1989). A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Systematic Zoology, 38, 7–25.CrossRefGoogle Scholar
Kluge, A. G. and Farris, J. S. (1969). Quantitative phyletics and evolution of anurans. Systematic Zoology, 18, 1–32.CrossRefGoogle Scholar
Kluge, A. G. and Wolf, A. J. (1993). Cladistics: what's in a word?Cladistics – The International Journal of the Willi Hennig Society, 9, 183–99.CrossRefGoogle Scholar
Maddison, W. P. (2000). Testing character correlation using pairwise comparisons on a phylogeny. Journal of Theoretical Biology, 202, 195–204.CrossRefGoogle ScholarPubMed
Marroig, G. and 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, 2576–600.CrossRefGoogle ScholarPubMed
Marroig, G., Vivo, M. and Cheverud, J. M. (2004). Cranial evolution in Sakis (Pithecia, Platyrrhini) ii: evolutionary processes and morphological integration. Journal of Evolutionary Biology, 17, 144–55.CrossRefGoogle ScholarPubMed
Moss, M. O. and Young, R. W. (1960). A functional approach to craniology. American Journal of Physical Anthropology, 18, 281–91.CrossRefGoogle ScholarPubMed
Myers, P. (2000). Carnivora (on-line), animal diversity web. .
Naylor, G. J. P. and Adams, D. C. (2001). Are the fossil data really at odds with the molecular data? Morphological evidence for Cetartiodactyla phylogeny reexamined. Systematic Biology, 50, 444–53.Google ScholarPubMed
Nowak, R. M. (1999). Walker's Mammals of the World, 6th ed. Baltimore, MD: Johns Hopkins University Press.Google Scholar
O'Keefe, F. R. and Wagner, P. J. (2001). Inferring and testing hypotheses of cladistic character dependence by using character compatibility. Systematic Biology, 50, 657–75.CrossRefGoogle ScholarPubMed
Olson, E. C. and Miller, R. L. (1951). A mathematical model applied to the evolution of species. Evolution, 5, 325–38.CrossRefGoogle Scholar
Olson, E. C. and Miller, R. L. (1958). Morphological Integration. Chicago, IL: University of Chicago Press.Google Scholar
Otto, S. P. and Day, T. (2007). A Biologist's Guide to Mathematical Modeling in Ecology and Evolution. Princeton, NJ: Princeton University Press.Google Scholar
Pigliucci, M. and Preston, K. (2004). Phenotypic Integration. Oxford: Oxford University Press.Google Scholar
Polly, P. D. (2005). Development and phenotypic correlations: the evolution of tooth shape in Sorex araneus. Evolution & Development, 7, 29–41.CrossRefGoogle ScholarPubMed
Polly, P. D., Head, J. J. and Cohn, M. J. (2001). Testing modularity and dissociation: the evolution of regional proportions in snakes. In Beyond Heterochrony: The Evolution of Development, ed. Zelditch, M. L.. New York, NY: Wiley-Liss, pp. 305–35.Google Scholar
Read, A. F. and Nee, S. (1995). Inference from binary comparative data. Journal of Theoretical Biology, 173, 99–108.CrossRefGoogle Scholar
Rieppel, O. and Kearney, M. (2002). Similarity. Biological Journal of the Linnean Society, 75, 59–82.CrossRefGoogle Scholar
Sadleir, R. W. and Makovicky, P. J. (2008). Cranial shape and correlated characters in crocodile evolution. Journal of Evolutionary Biology, 21, 1578–96.CrossRefGoogle ScholarPubMed
Sanchez-Villagra, M. R. and Williams, B. (1998). Levels of homoplasy in the evolution of the mammalian skeleton. Journal of Mammalian Evolution, 5, 113–26.CrossRefGoogle Scholar
Schlosser, G. and Wagner, G. P. (2004). Modularity in Development and Evolution. Chicago, IL: University of Chicago Press.Google Scholar
Schwenk, K. (2001). Functional units and their evolution. In The Character Concept in Evolutionary Biology, ed. Wagner, G. P.. San Diego, CA: Academic Press, pp. 165–98.CrossRefGoogle Scholar
Shubin, N. and Davis, M. C. (2004). Modularity in the evolution of vertebrate appendages. In Modularity in Development and Evolution, ed. Schlosser, G. and Wagner, G. P.. Chicago, IL: University of Chicago Press, pp. 429–40.Google Scholar
Steppan, S. J. (1997). Phylogenetic analysis of phenotypic covariance structure. II. Reconstructing matrix evolution. Evolution, 51, 587–94.CrossRefGoogle ScholarPubMed
Strait, D. S. (2001). Integration, phylogeny, and the hominid cranial base. American Journal of Physical Anthropology, 114, 273–97.CrossRefGoogle ScholarPubMed
Tedford, R. H., Taylor, B. E. and Wang, X. (1995). Phylogeny of the Canidae (Carnivora: Canidae): the living taxa. American Museum Novitates, 3146, 1–37.Google Scholar
Thorogood, P. (1993). Differentiation and morphogenesis of cranial skeletal tissues. In The Skull, ed. Hanken, J. and Hall, B. K.. Chicago, IL: University of Chicago Press, pp. 112–52.Google Scholar
Van Der Klaauw, C. J. (1948–1952). Size and position of the functional components of the skull. Archives Neerlandaises de Zoologie, 9, 1–559.CrossRefGoogle Scholar
Vermeij, G. J. (1973). Adaptation, versatility, and evolution. Systematic Zoology, 22, 466–77.CrossRefGoogle Scholar
Wagner, G. P. (1995). Adaptation and the modular design of organisms. Advances in Artificial Life, 929, 317–28.Google Scholar
Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36, 36–43.CrossRefGoogle Scholar
Wagner, G. P. and Altenberg, L. (1996). Perspective: complex adaptations and the evolution of evolvability. Evolution, 50, 967–76.CrossRefGoogle ScholarPubMed
Wagner, P. J. (1998). A likelihood approach for evaluating estimates of phylogenetic relationships among fossil taxa. Palaeobiology, 24, 430–49.CrossRefGoogle Scholar
Wesley-Hunt, G. D. and Flynn, J. J. (2005). Phylogeny of the Carnivora: basal relationships among the carnivoramorphans, and assessment of the position of ‘Miacoidea’ relative to crown-clade Carnivora. Journal of Systematic Palaeontology, 3, 1–28.CrossRefGoogle Scholar
Williams, B. (2007). Comparing levels of homoplasy in the primate skeleton. Journal of Human Evolution, 52, 480–89.CrossRefGoogle ScholarPubMed
Wyss, A. R. and Flynn, J. J. (1993). A phylogenetic analysis and definition of the carnivora. In Mammal Phylogeny, ed. Szalay, F. S., Novacek, M. J. and McKenna, M. C.. New York, NY: Springer, pp. 32–52.CrossRefGoogle Scholar
Yoder, A. D., Burns, M. M., Zehr, S., et al. (2003). Single origin of Malagasy Carnivora from an African ancestor. Nature, 421, 734–37.CrossRefGoogle ScholarPubMed
Zelditch, M. L. (1988). Ontogenetic variation in patterns of phenotypic integration in the laboratory rat. Evolution, 42, 28–41.CrossRefGoogle ScholarPubMed
Zelditch, M. L. and Carmichael, A. C. (1989a). Growth and intensity of integration through postnatal growth in the skull of Sigmodon fulviventer. Journal of Mammalogy, 70, 477–84.CrossRefGoogle Scholar
Zelditch, M. L. and Carmichael, A. C. (1989b). Ontogenetic variation in patterns of developmental and functional integration in skulls of Sigmodon fuliviventer. Evolution, 43, 814–24.CrossRefGoogle Scholar
Zelditch, M. L., Sheets, H. D. and Fink, W. L. (2001). The spatial complexity and evolutionary dynamics of growth. In Beyond Heterochrony: The Evolution of Development, ed. Zelditch, M. L.. New York, NY: Wiley-Liss, pp. 145–94.Google Scholar

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