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Principal component analysis of avian hind limb and foot morphometrics and the relationship between ecology and phylogeny

Published online by Cambridge University Press:  23 September 2020

Amanda R. Falk Open the ORCID record for Amanda R. Falk [Opens in a new window] ,
James C. Lamsdell Open the ORCID record for James C. Lamsdell [Opens in a new window]  and
Enpu Gong
Amanda R. Falk*
Affiliation:
Biology Program, Centre College, 600 West Walnut Street, Danville, Kentucky40422, U.S.A. E-mail: amanda.falk@centre.edu
James C. Lamsdell
Affiliation:
Department of Geology and Geography, West Virginia University, Morgantown, West Virginia26506, U.S.A. E-mail: james.lamsdell@mail.wvu.edu
Enpu Gong
Affiliation:
Northeastern University, Department of Geology, Shenyang, Liaoning110819, China. E-mail: gongep@mail.neu.edu.cn
*
*Corresponding author.
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Abstract

Principal component analysis has been used to test for similarities in ecology and life habit between modern and fossil birds; however, the two main portions of the hind limb—the foot and the long bone elements—have not been examined separately. We examine the potential links between morphology, ecology, and phylogeny through a synthesis of phylogenetic paleoecological methods and morphospace analysis. Both hind limb morphologies and species’ ecologies exhibit extreme phylogenetic clumping, although these patterns are at least partially explainable by a Brownian motion style of evolution. Some morphologies are strongly correlated with particular ecologies, while some ecologies are occupied by a variety of morphologies. Within the morphospace analyses, the length of the hallux (toe I) is the most defining characteristic of the entire hind limb. The foot and hind limb are represented on different axes when all measurements are considered in an analysis, suggesting that these structures undergo morphological change separately from each other. Early birds tend to cluster together, representing an unspecialized basal foot morphotype and a hind limb reliant on hip-driven, not knee-driven, locomotion. Direct links between morphology, ecology, and phylogeny are unclear and complicated and may be biased due to sample size (~60 species). This study should be treated as a preliminary analysis that further studies, especially those examining the vast diversity of modern birds, can build upon.

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Articles
Information
Paleobiology , Volume 47 , Special Issue 2: Phylogenetic Paleoecology , March 2021 , pp. 314 - 336
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press on behalf of The Paleontological Society

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Footnotes

Data available from the Dryad Digital Repository:https://doi.org/10.5061/dryad.dr7sqv9wb.

*Corresponding author.

References

Literature Cited

Anten-Houston, M. V., Ruta, M., and Deeming, D. C.. 2017. Effects of phylogeny and locomotor style on the allometry of body mass and pelvic dimensions in birds. Journal of Anatomy 231:342–358.Google ScholarPubMed
Baker, A. J., Pereira, S. L., and Paton, T. A.. 2007. Phylogenetic relationships and divergence times of Charadriiformes genera: multigene evidence of the Cretaceous origin of at least 14 clades of shorebirds. Biology Letters 3:205–210.CrossRefGoogle ScholarPubMed
Barbosa, A., and Moreno, E.. 1999a. Evolution of foraging strategies in shorebirds: an ecomorphological approach. The Auk 116:712–725.Google Scholar
Barbosa, A., and Moreno, E.. 1999b. Hindlimb morphology and locomotor performance in waders: an evolutionary approach. Biological Journal of the Linnean Society 67:313–330.Google Scholar
Barth, J. M. I., Matschiner, M., and Robertson, B. C.. 2013. Phylogenetic position and subspecies divergence of the endangered New Zealand dotterel (Charadrius obscurus). PLoS ONE 8:e78068.Google Scholar
Bell, A., and Chiappe, L. M.. 2011. Statistical approach for inferring ecology of Mesozoic birds. Journal of Systematic Palaeontology 9:119–133.Google Scholar
Burin, G., Kissling, W. D., Guimarães, P. R. Jr., Şekercioğlu, C. H., and Quental, T. B.. 2016. Omnivory in birds is a macroevolutionary sink. Nature Communications 7:11250.10.1038/ncomms11250CrossRefGoogle ScholarPubMed
Carrier, D. R., and Farmer, C. G.. 2000. The integration of ventilation and locomotion in Archosaurs. American Zoologist 40:87–100.Google Scholar
Chiappe, L. M., and Walker, C. A.. 2002. Skeletal morphology and systematics of the Cretaceous Euenantiornithes (Ornithothoraces: Enantiornithes). Pp. 240–267 in Chiappe, L. M. and Witmer, L. M., eds. Mesozoic birds: above the heads of dinosaurs. University of California Press, Berkeley.Google Scholar
Chiappe, L. M., Zhao, B., O'Connor, J. K., Gao, C., Wang, X., Habib, M., Marugan-Lobon, J., Meng, Q., and Cheng, X.. 2017. A new specimen of the Early Cretaceous bird Hongshanornis longicresta: insights into the aerodynamics and diet of a basal ornithuromorph. PeerJ 2:e234.CrossRefGoogle Scholar
Dececchi, T. A., and Larsson, H. C. E.. 2011. Assessing arboreal adaptations of bird antecedents: testing the ecological setting of the origin of the avian flight stroke. PLoS One 6: e22292.Google ScholarPubMed
DeGrange, F. J. 2017. Hind limb morphometry of terror birds (Aves, Cariamiformes, Phorusrhacidae): functional implications for substrate preferences and locomotor lifestyle. Transactions of the Royal Society of Edinburgh (Earth and Environmental Science) 106:257–276.Google Scholar
Elliott, A. 1992. Pelecanidae. Pp. 290–311 in Hoyo, J. Del, Elliott, A., and Sargatal, J., eds. Handbook of the birds of the world, Vol. 1. Ostrich to ducks. Lynx Edicions, Barcelona.Google Scholar
Fowler, D. W., Freedman, E. A., Scannella, J. B., and Kambic, R. E.. 2011. The predatory ecology of Deinonychus and the origin of flapping in birds. PLoS ONE 12: e28964.CrossRefGoogle Scholar
Fritz, S. A., and Purvis, A.. 2010. Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conservation Biology 24:1042–1051.CrossRefGoogle ScholarPubMed
Garcia-R, J. C., Gibb, G. C., and Trewick, S. A.. 2014. Deep global evolutionary radiation in birds: diversification and trait evolution in the cosmopolitan bird family Rallidae. Molecular Phylogenetics and Evolution 81:96–108.Google ScholarPubMed
Gatesy, S. M., and Middleton, K. M.. 1997. Bipedalism, flight, and the evolution of theropod locomotor diversity. Journal of Vertebrate Paleontology 17:308–329.CrossRefGoogle Scholar
Gibson, R., and Baker, A.. 2012. Multiple gene sequences resolve phylogenetic relationships in the shorebird suborder Scolopaci (Aves: Charadriiformes). Molecular Phylogenetics and Evolution 64:66–72.CrossRefGoogle Scholar
Glen, C. L., and Bennet, M. B.. 2007. Foraging modes of Mesozoic birds and non-avian therapods. Current Biology 17:R911–R912.CrossRefGoogle Scholar
Habib, M. B., and Ruff, C. B.. 2008. The effects of locomotion on the structural characteristics of avian limb bones. Zoological Journal of the Linnean Society 153:601–624.Google Scholar
Hall, J. C., Braham, M. A., Nolan, L. A., Conley, J., Brandt, J., Mendenhall, L., Lanzone, M., McGann, A., and Katzner, T. E.. 2019. Characteristics of feeding sites of California condors (Gymnogyps californianus) in the human-dominated landscape of southern California. Wilson Journal of Ornithology 131:459–471.Google Scholar
Hammer, Ø., and Harper, D. A. T.. 2005. Palaeontological data analysis. Blackwell, Oxford.Google Scholar
Hertel, F., and Campbell, K. E.. 2007. The antitrochanter of birds: form and function in balance. The Auk 124:789–805.CrossRefGoogle Scholar
Hieronymous, T. L. 2015. Qualitative skeletal correlates of wing shape in extant birds (Aves: Neoaves). BMC Evolutionary Biology 15:30.CrossRefGoogle Scholar
Hopkins, M. J. 2016. Magnitude versus direction of change and the contribution of macroevolutionary trends to morphological disparity. Biological Journal of the Linnean Society 118:116–130.Google Scholar
Hopson, J. A. 2001. Ecomorphology of avian and nonavian theropod phalangeal proportions: Implications for the arboreal versus terrestrial origin of bird flight. Pp. 211–235 in Gauthier, J. and Gall, L. F., eds. New perspectives on the origin and early evolution of birds. Yale University Peabody Museum, New Haven, Conn.Google Scholar
Hutchinson, J. R., and Allen, V.. 2009. The evolutionary continuum of limb function from early theropods to birds. Naturwissenschaften 96:423–448.Google ScholarPubMed
Jarvis, E. D., Mirarab, S., Aberer, A. J., Li, B., Houde, P., Li, C., Hou, S. Y. W., et al. . 2014. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346:1320–1331.Google ScholarPubMed
Lamsdell, J. C. 2016. Horseshoe crab phylogeny and independent colonizations of fresh water: ecological invasion as a driver for morphological innovation. Palaeontology 59:181–194.Google Scholar
Lamsdell, J. C., Congreve, C. R., Hopkins, M. J., Krug, A. Z., and Patzkowsky, M. E.. 2017. Phylogenetic paleoecology: tree-thinking and ecology in deep time. Trends in Ecology and Evolution 32:452–463.Google ScholarPubMed
Livezey, B. C., and Zusi, R. L.. 2007. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zoological Journal of the Linnean Society 149:1–95.Google ScholarPubMed
Mackey, D. L. 1984. Roosting habitat of Merriam's turkeys in south-central Washington. Journal of Wildlife Management 38:1377–1382.CrossRefGoogle Scholar
Mackiewicz, P., Urantówka, A. D., Kroczak, A., and Mackiewicz, D.. 2019. Resolving phylogenetic relationships within Passeriformes based on mitochondrial genes and inferring the evolution of their mitogenomes in terms of duplications. Genome Biology and Evolution 11:2824–2849.CrossRefGoogle ScholarPubMed
Middleton, K. M. 2001. The morphological basis of hallucal orientation in extant birds. Journal of Morphology 250:51–60.Google ScholarPubMed
Middleton, K. M., and Gatesy, S. M.. 2000. Theropod forelimb design and evolution. Zoological Journal of the Linnean Society 128:149–187.CrossRefGoogle Scholar
Miles, D. B. 1990. The importance and consequences of temporal variation in avian foraging behavior. Studies in Avian Biology 13:210–217.Google Scholar
Mosto, M. C. 2017. Comparative hindlimb myology within the family Falconidae. Zoomorphology 136:241–250.CrossRefGoogle Scholar
Myer, G. 2008. Avian higher-level phylogeny: well-supported clades and what we can learn from a phylogenetic analysis of 2954 morphological characters. Journal of Zoological Systematics and Evolutionary Research 46:63–72.Google Scholar
Nudds, R. L., Atterholt, J., Wang, H-L., and Dyke, G. J.. 2013. Locomotory abilities and habitat of the Cretaceous bird Gansus yumenensis inferred from limb length proportions. Journal of Evolutionary Biology 26:150–154.Google ScholarPubMed
O'Connor, J. K., Wang, X., Chiappe, L. M., Gao, C., Meng, Q., Cheng, X., and Liu, J.. 2009. Phylogenetic support for a specialized clade of Cretaceous enantiornithine birds with information from a new species. Journal of Vertebrate Paleontology 29:188–204.CrossRefGoogle Scholar
O'Connor, J. K., Chiappe, L. M., Gao, C., and Zhao, B.. 2011. Anatomy of the Early Cretaceous enantiornithine bird Rapaxavis pani. Acta Palaeontologica Polonica 56:463–475.Google Scholar
Orme, D., Freckleton, R., Thomas, G., Petzoldt, T., Fritz, S., Isaac, N., and Pearse, W. D.. 2013. Caper: comparative analyses of phylogenetics and evolution in R. https://CRAN.R-project.org/package=caper.Google Scholar
Pereira, S. L., and Baker, A. J.. 2008. DNA evidence for a Paleocene origin of the Alcidae (Aves: Charadriiformes) in the Pacific and multiple dispersals across northern oceans. Molecular Phylogenetics and Evolution 46:430–445.CrossRefGoogle ScholarPubMed
Prum, R. O., Berv, J. S., Dornburg, A., Field, D. J., Townsend, J. P., Lemmon, E. M., and Lemmon, A. R.. 2015. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526:569–573.Google ScholarPubMed
R Core Team. 2018. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org.Google Scholar
Revell, L. J. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3:217–223.Google Scholar
Rubinson, J., Lloyd, D. G., Besier, T. F., Heliams, D. B., and Fournier, P. A.. 2007. Running in ostriches (Struthio camelus): three-dimensional joint axes alignment and joint kinematics. Journal of Experimental Biology 210:2548–2562.Google Scholar
Serrano, F. J., Chiappe, L. M., Palmqvist, P., Figueirido, B., Marugán-Lobón, J., and Sanz, J. L.. 2018. Flight reconstruction of two European enantiornithines (Aves, Pygostylia) and the achievement of bounding flight in Early Cretaceous birds. Paleontology 61:359–368.CrossRefGoogle Scholar
Sexton, J. P., Montiel, J., Shay, J. E., Stephens, M. R., and Slatyer, R. A. 2017. Evolution of ecological niche breadth. Annual Review of Ecology, Evolution, and Systematics 48:183–206.Google Scholar
Sibley, D. A. 2000. The Sibley guide to birds, 3rd ed. Knopf, New York.Google Scholar
Stoessel, A., and Fischer, M. S.. 2012. Comparative intralimb coordination in avian bipedal locomotion. Journal of Experimental Biology 215:4055–4069.Google ScholarPubMed
Sun, Z., Pan, T., Hu, C., Sun, L., Ding, H., Wang, H., Zhang, C., et al. . 2017. Rapid and recent diversification patterns in Anseriformes birds: inferred from molecular phylogeny and diversification analyses. PLoS ONE 12:e0184529.CrossRefGoogle ScholarPubMed
Udeh, I., and Ogbu, C.. 2011. Principal component analysis of body measurements in three strains of broiler chicken. Science World Journal 6(2):11–14.Google Scholar
Verma, D., Sankhyan, V., Katoch, S., and Thakur, Y. P.. 2015. Principal component analysis of biometric traits to reveal body confirmation in local hill cattle of Himalayan state of Himachal Pradesh, India. Veterinary World 8:1453–1457.Google ScholarPubMed
Vohra, V., Niranjan, S. K., Mishra, A. K., Jamuna, V., Chopra, A., Sharma, N., and Jeong, D. K.. 2015. Phenotypic characterization and multivariate analysis to explain body conformation in lesser known buffalo (Bubalus bubalis) from North India. Asian-Australasian Journal of Animal Sciences 23:311–317.Google Scholar
Wang, M., O'Connor, J. K., Pan, Y., and Zhou, Z.. 2017. A bizarre Early Cretaceous enantiornithine bird with unique crural feathers and an ornithuromorph plough-shaped pygostyle. Nature Communications 8:14141.Google Scholar
Wang, X., McGowan, A. J., and Dyke, G. J.. 2011. Avian wing proportions and flight styles: first step towards predicting the flight modes of Mesozoic birds. PLoS ONE 6: e28672.Google ScholarPubMed
Wang, X., O'Connor, J. K., Zheng, X., Wang, M., Hu, H., and Zhou, Z.. 2014. Insights into the evolution of rachis dominated tail feathers from a new basal enantiornithine (Aves: Ornithothoraces). Biological Journal of the Linnean Society 113:805–819.Google Scholar
Worth, C. B. 1943. Notes on the chimney swift. The Auk 60:558–564.Google Scholar
Xu, X., Zhou, Z., Dudley, R., Mackem, S., Chung, C.-M., Erickson, G. M., and Varricchio, D. J.. 2014. An integrative approach to understanding bird origins. Science 346:1341.Google ScholarPubMed
You, H., Lamanna, M. C., Harris, J. D., Chiappe, L. M., O'Connor, J. K., Ji, S., Lü, J., et al. 2006. A nearly modern amphibious bird from the Early Cretaceous of northwestern China. Science 312:1640–1643.CrossRefGoogle ScholarPubMed
Zeffer, A., Johansson, L. C., and Marmebro, A.. 2003. Functional correlation between habitat use and leg morphology in birds (Aves). Biological Journal of the Linnean Society 79:461–484.Google Scholar
Zhou, Z., and Zhang, F.. 2005. Discovery of an ornithurine bird and its implication for Early Cretaceous avian radiation. Proceedings of the National Academy of Sciences USA 102:18998–19002.Google ScholarPubMed