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Modularity of the Neck in Birds (Aves)

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Abstract

The neck connects the head and the trunk and is the key structure allowing all movements of the head. The neck morphology of birds is the most variable among living tetrapods, including significant differences in the number and shape of the cervical vertebrae. Despite these differences, according to the literature, three morphofunctional regions (i.e., modules) have been identified along the neck. However, this regionalization has not been quantitatively tested through a geometric morphometric approach applied to the cervical vertebrae. Based on the examination of 187 cervical vertebrae belonging to 16 species with various ecologies, we revealed a common modular structure of the neck using 3D surface geometric morphometrics. We adopted an approach without a priori clustering to identify modules along the neck. The phylogenetic influence on each module was tested. Then, each module was digitally reconstructed as a 3D vertebral model, and postural characteristics were studied. We characterized 9 modules: 7 are transpecific, being shared by at least 2 and up to 15 species. Two modules are specific to species with particularly long necks. The modularity pattern appears to be tightly linked to morphofunctional aspects and partially to phylogeny. In contrast, feeding ecology seems to be more closely related to the chaining of modules (the neck) than to the modules themselves. A study of postural properties revealed that each modular unit exhibits a characteristic curvature. Overall, the modular structure of the neck corresponds to the three traditional functional regions. However, the results also revealed unexpected pattern complexity, including subdivisions within these regions. The study of the patterns of modularity is therefore a relevant approach for challenging the three-functional-region hypothesis and allowed us to identify the structure of the diversity of the necks of birds.

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References

  • Adams, D. C. (2014). A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Systematic Biology,63(5), 685–697.

    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(4), 393–399.

    Article  Google Scholar 

  • Alexander, R. M. (1985). Mechanics of posture and gait of some large dinosaurs. Zoological Journal of the Linnean Society,83(1), 1–25.

    Article  Google Scholar 

  • Arnold, P., Esteve-Altava, B., & Fischer, M. S. (2017). Musculoskeletal networks reveal topological disparity in mammalian neck evolution. BMC Evolutionary Biology,17(1), 251.

    Article  PubMed  PubMed Central  Google Scholar 

  • Arnold, P., Forterre, F., Lang, J., & Fischer, M. S. (2016). Morphological disparity, conservatism, and integration in the canine lower cervical spine: Insights into mammalian neck function and regionalization. Mammalian Biology,81(2), 153–162.

    Article  Google Scholar 

  • Asher, R. J., Lin, K. H., Kardjilov, N., & Hautier, L. (2011). Variability and constraint in the mammalian vertebral column: Mammalian vertebral variability. Journal of Evolutionary Biology,24(5), 1080–1090.

    Article  CAS  PubMed  Google Scholar 

  • Baylac, M., & Frieß, M. (2005). Fourier descriptors, procrustes superimposition, and data dimensionality: An example of cranial shape analysis in modern human populations. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 145–165). Boston: Springer.

    Chapter  Google Scholar 

  • Baylac, M., Villemant, C., & Simbolotti, G. (2003). Combining geometric morphometrics with pattern recognition for the investigation of species complexes: Geometric morphometrics, pattern recognition and species complexes. Biological Journal of the Linnean Society,80(1), 89–98.

    Article  Google Scholar 

  • Blender Foundation (2003–2018). Blender. Stichting Blender Foundation, Amsterdam, https://www.blender.org

  • Blomberg, S. P., Garland, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioural traits are more labile. Evolution,57(4), 717–745.

    Article  PubMed  Google Scholar 

  • Boas, J. E. V. (1929). Biologisch-anatomische Studien über den Hals der Vögel (pp. 1–127). Köbenhavn: A.F. Host & Son.

    Google Scholar 

  • Böhmer, C., Plateau, O., Cornette, R., & Abourachid, A. (2019). Correlated evolution of neck length and leg length in birds. Royal Society open science,6(5), 181588.

    Article  PubMed  PubMed Central  Google Scholar 

  • Böhmer, C., Rauhut, O. W. M., & Wörheide, G. (2015). Correlation between Hox code and vertebral morphology in archosaurs. Proceedings of the Royal Society B: Biological Sciences,282(1810), 20150077.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bookstein, F. L. (1997). Morphometric tools for landmarks data: geometry and biology. Cambridge: Cambridge University Press.

    Google Scholar 

  • Botton-Divet, L., Houssaye, A., Herrel, A., Fabre, A.-C., & Cornette, R. (2015). Tools for quantitative form description; an evaluation of different software packages for semi-landmark analysis. PeerJ,3, e1417.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bout, R. G. (1997). Postures of the avian craniocervical column. Journal of Morphology,231, 287–295.

    Article  CAS  PubMed  Google Scholar 

  • Brocklehurst, R. J., Schachner, E. R., & Sellers, W. I. (2018). Vertebral morphometrics and lung structure in non-avian dinosaurs. Royal Society Open Science,5(10), 180983.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheverud, J. M. (1996). Developmental integration and the evolution of pleiotropy. American Zoologist,36(1), 44–50.

    Article  Google Scholar 

  • Cobley, M. J., Rayfield, E. J., & Barrett, P. M. (2013). Inter-vertebral flexibility of the ostrich neck: Implications for estimating sauropod neck flexibility. PLoS ONE,8(8), e72187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cordeiro-Estrela, P., Baylac, M., Denys, C., & Marinho-Filho, J. (2006). Interspecific patterns of skull variation between sympatric Brazillian vesper mice: Geometric morphometrics assessment. Journal of Mammalogy,87(6), 1270–1279.

    Article  Google Scholar 

  • Cornette, R., Baylac, M., Souter, T., & Herrel, A. (2013). Does shape co-variation between the skull and the mandible have functional consequences? A 3D approach for a 3D problem. Journal of Anatomy,223(4), 329–336.

    Article  PubMed  PubMed Central  Google Scholar 

  • Daeschler, E. B., Shubin, N. H., & Jenkins, F. A. (2006). A Devonian tetrapod-like fish and the evolution of the tetrapod body plan. Nature,440(7085), 757–763.

    Article  CAS  PubMed  Google Scholar 

  • Dasgupta, A., & Raftery, A. E. (1998). Detecting features in spatial point processes with clutter via model-based clustering. Journal of the American statistical Association,93, 294–302.

    Article  Google Scholar 

  • de Azevedo, T. P., Witten, P. E., Huysseune, A., Bensimon-Brito, A., Winkler, C., To, T. T., et al. (2012). Interrelationship and modularity of notochord and somites: A comparative view on zebrafish and chicken vertebral body development: Modularity of notochord and somites in zebrafish and chicken. Journal of Applied Ichthyology,28(3), 316–319.

    Article  Google Scholar 

  • Diaconis, P., & Freedman, D. (1984). Asymptotics of graphical projection pursuit. The Annals of Statistics,12(3), 793–815.

    Article  Google Scholar 

  • Dilger, W. C. (2010). The comparative ethology of the African Parrot Genus Agapornis. Zeitschrift Für Tierpsychologie,17(6), 649–685.

    Article  Google Scholar 

  • Ericsson, R., Knight, R., & Johanson, Z. (2013). Evolution and development of the vertebrate neck. Journal of Anatomy,222(1), 67–78.

    Article  PubMed  Google Scholar 

  • Everitt, B., & Dunn, G. (2001). Applied multivariate data analysis (2nd ed.). Chichester: Wiley.

    Book  Google Scholar 

  • Fraley, C., & Raftery, A. E. (1998). How many clusters? Which clustering meSthod? Answers via model-based cluster analysis. The Computer Journal,41(8), 578–588.

    Article  Google Scholar 

  • Fraley, C., & Raftery, A. E. (2012). mclust Version 4 for R: Normal mixture modeling for model-based clustering, classification, and density estimation. Department of Statistics, University of Washington, Technical Report no. 597.

  • Galis, F. (1999). Why do almost all mammals have seven cervical vertebrae? Developmental constraints, Hox genes, and cancer. Journal of Experimental Zoology,285(1), 19–26.

    Article  CAS  PubMed  Google Scholar 

  • Graf, W., Waele, C. D., & Vidal, P. P. (1994). Functional anatomy of the head-neck movement system of quadrupedal and bipedal mammals. Journal of Anatomy,186, 55–74.

    Google Scholar 

  • Guinard, G. (2012). Evolutionary concepts meet the neck of penguins (Aves: Sphenisciformes), towards a “survival strategy” for evo-devo. Theory in Biosciences,131(4), 231–242.

    Article  PubMed  Google Scholar 

  • Guinard, G., & Marchand, D. (2010). Modularity and Complete Natural Homeoses in Cervical Vertebrae of Extant and Extinct Penguins (Aves: Sphenisciformes). Evolutionary Biology,37(4), 210–226.

    Article  Google Scholar 

  • Guinard, G., Marchand, D., Courant, F., Gauthier-Clerc, M., & Le Bohec, C. (2010). Morphology, ontogenesis and mechanics of cervical vertebrae in four species of penguins (Aves: Spheniscidae). Polar Biology,33(6), 807–822.

    Article  Google Scholar 

  • Gunz, P., Mitteroecker, P., & Bookstein, F. L. (2005). Semilandmarks in three dimensions. In D. E. Slice (Ed.), Modern morphometrics in physical anthropology (pp. 73–98). Boston: Springer.

    Chapter  Google Scholar 

  • Hackett, S. J., Kimball, R. T., Reddy, S., Bowie, R. C. K., Braun, E. L., Braun, M. J., et al. (2008). A Phylogenomic study of birds reveals their evolutionary history. Science,320(5884), 1763–1768.

    Article  CAS  PubMed  Google Scholar 

  • Hallgrímsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., et al. (2009). Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology,36(4), 355–376.

    Article  PubMed  Google Scholar 

  • Harmon, L. J., Weir, J. T., Brock, C. D., Glor, R. E., & Challenger, W. (2008). GEIGER: Investigating evolutionary radiations. Bioinformatics,24(1), 129–131.

    Article  CAS  PubMed  Google Scholar 

  • Hautier, L., Weisbecker, V., Sanchez-Villagra, M. R., Goswami, A., & Asher, R. J. (2010). Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proceedings of the National Academy of Sciences,107(44), 18903–18908.

    Article  CAS  Google Scholar 

  • Head, J. J., & Polly, P. D. (2015). Evolution of the snake body form reveals homoplasy in amniote Hox gene function. Nature,520, 86–89.

    Article  CAS  PubMed  Google Scholar 

  • Heidweiller, J., Van Der Leeuw, A. H. J., & Zweers, G. A. (1992). Cervical kinematics during drinking in developing chickens. Journal of Experimental Zoology,262(2), 135–153.

    Article  CAS  PubMed  Google Scholar 

  • Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K., & Mooers, A. O. (2012). The global diversity of birds in space and time. Nature,491(7424), 444–448.

    Article  CAS  PubMed  Google Scholar 

  • Johnson, S. E., & Shapiro, L. J. (1998). Positional behavior and vertebral morphology in atelines and cebines. American Journal of Physical Anthropology,105, 333–354.

    Article  CAS  PubMed  Google Scholar 

  • Jones, K. E., Angielczyk, K., & Pierce, S. (2019). Vertebral regionalization facilitates functional diversification of the mammalian axial skeleton. The FASEB Journal,33, 613.

    Google Scholar 

  • Jones, K. E., Benitez, L., Angielczyk, K. D., & Pierce, S. E. (2018). Adaptation and constraint in the evolution of the mammalian backbone. BMC Evolutionary Biology,18(1), 172.

    Article  PubMed  PubMed Central  Google Scholar 

  • Long, J. H., Pabst, D. A., Shepherd, W. R., & Mclellan, W. A. (1997). Locomotor desing of dolphin vertebral columns: bending mechanics and morphology of Dolphinus delphis. The Journal of Experimental Biology,200, 65–81.

    PubMed  Google Scholar 

  • Kambic, R. E., Biewener, A. A., & Pierce, S. E. (2017). Experimental determination of three-dimensional cervical joint mobility in the avian neck. Frontiers in Zoology,14(1), 37.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kembel, S. W., Cowan, P. D., Helmus, M. R., Cornwell, W. K., Morlon, H., Ackerly, D. D., et al. (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics,26(11), 1463–1464.

    Article  CAS  PubMed  Google Scholar 

  • Klingenberg, C. P. (2008). Morphological Integration and Developmental Modularity. Annual Review of Ecology, Evolution, and Systematics,39(1), 115–132.

    Article  Google Scholar 

  • Klingenberg, C. P. (2010). Evolution and development of shape: integrating quantitative approaches. Nature Reviews Genetics,11, 623–635.

    Article  CAS  PubMed  Google Scholar 

  • Klingenberg, C. P. (2014). Studying morphological integration and modularity at multiple levels: Concepts and analysis. Philosophical Transactions of the Royal Society B: Biological Sciences,369(1649), 20130249–20130249.

    Article  Google Scholar 

  • Klingenberg, C. P., & Marugán-Lobón, J. (2013). Evolutionary covariation in geometric morphometric data: Analyzing integration, modularity, and allometry in a phylogenetic context. Systematic Biology,62(4), 591–610.

    Article  PubMed  Google Scholar 

  • Krings, M., Nyakatura, J. A., Boumans, M. L. L. M., Fischer, M. S., & Wagner, H. (2017). Barn owls maximize head rotations by a combination of yawing and rolling in functionally diverse regions of the neck. Journal of Anatomy,231(1), 12–22.

    Article  PubMed  PubMed Central  Google Scholar 

  • Krings, M., Nyakatura, J. A., Fischer, M. S., & Wagner, H. (2014). The cervical spine of the american barn owl (Tyto furcata pratincola): I. Anatomy of the vertebrae and regionalization in their S-shaped arrangement. PLoS ONE,9(3), e91653.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Muller, J., Scheyer, T. M., Head, J. J., Barrett, P. M., Werneburg, I., Ericson, P. G. P., et al. (2010). Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes. Proceedings of the National Academy of Sciences,107(5), 2118–2123.

    Article  Google Scholar 

  • Oliver, J. D., Jones, K. E., Hautier, L., Loughry, W. J., & Pierce, S. E. (2016). Vertebral bending mechanics and xenarthrous morphology in the nine-banded armadillo (Dasypus novemcinctus). The Journal of Experimental Biology,219(19), 2991–3002.

    Article  PubMed  Google Scholar 

  • Olson, E. C., & Miller, R. L. (1958). Morphological integration. Chicago: University of Chicago Press.

    Google Scholar 

  • Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics,20(2), 289–290.

    Article  CAS  PubMed  Google Scholar 

  • Pierce, S. E., Ahlberg, P. E., Hutchinson, J. R., Molnar, J. L., Sanchez, S., Tafforeau, P., et al. (2013). Vertebral architecture in the earliest stem tetrapods. Nature,494(7436), 226–229.

    Article  CAS  PubMed  Google Scholar 

  • Polly, P. D., Head, J. J., & Cohn, M. J. (2001). Testing modularity and dissociation: the evolution of regional proportions in snakes. In M. L. Zelditch (Ed.), Beyond heterochrony: The evolution of development (pp. 305–335). New York: Wiley.

    Google Scholar 

  • R Core Team. (2017). R: A language and environment for statistical computing. Retrieved April 2, 2018, from https://www.R-project.org/.

  • Randau, M., Cuff, A. R., Hutchinson, J. R., Pierce, S. E., & Goswami, A. (2017). Regional differentiation of felid vertebral column evolution: A study of 3D shape trajectories. Organisms Diversity & Evolution,17(1), 305–319.

    Article  Google Scholar 

  • Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things): Phytools: R package. Methods in Ecology and Evolution,3(2), 217–223.

    Article  Google Scholar 

  • Riedl, R. (1978). Order in living organisms: a systems analysis of evolution. New York: Wiley.

    Google Scholar 

  • Rohlf, F. J., & Slice, D. (1990). Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Zoology,39(1), 40.

    Article  Google Scholar 

  • Romer, A. S. (1950). The vertebrate body. Philadelphia: W. B. Saunders Company.

    Google Scholar 

  • Shapiro, L. J., & Kemp, A. D. (2019). Functional and developmental influences on intraspecific variation in catarrhine vertebrae. American Journal of Physical Anthropology,168(1), 131–144.

    Article  PubMed  Google Scholar 

  • Schlager, S. (2013). Morpho: Calculations and visualisations related to geometric morphometrics. Retrieved April 2, 2018, from https://sourceforge.net/projects/morpho-rpackage/.

  • Stevens, K. A., & Parrish, J. M. (1999). Neck Posture and feeding habits of two jurassic sauropod dinosaurs. Science,284(5415), 798–800.

    Article  CAS  PubMed  Google Scholar 

  • Tambussi, C. P., de Mendoza, R., Degrange, F. J., & Picasso, M. B. (2012). Flexibility along the neck of the neogene terror bird Andalgalornis steulleti (Aves Phorusrhacidae). PLoS ONE,7(5), e37701.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Leeuw, H. J., Bout, R. G., & Zweers, G. A. (2001). Control of the cranio-cervical system during feeding in birds. American Zoologist,41, 1352–1363.

    Google Scholar 

  • Villamil, C. I. (2018). Phenotypic integration of the cervical vertebrae in the Hominoidea (Primates): Cervical vertebrae integration in Apes. Evolution,72(3), 490–517.

    Article  PubMed  Google Scholar 

  • Virchow, H. (1910). Über die Bewegungsmöglichkeiten an der Wirbelsäule von Spheniscus. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin. 1: 4–19.

  • Werneburg, I., Wilson, L. A. B., Parr, W. C. H., & Joyce, W. G. (2015). Evolution of neck vertebral shape and neck retraction at the transition to modern turtles: An integrated geometric morphometric approach. Systematic Biology,64(2), 187–204.

    Article  PubMed  Google Scholar 

  • West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford: Oxford University Press.

    Google Scholar 

  • Wickham, H. (2015). ggplot2: Elegant graphics for data analysis. Berlin: Springer.

    Google Scholar 

  • Wiley, D. F., Amenta, N., Alcantara, D. A., Ghosh, D., Kil, Y. J., Delson, E., et al. (2005). Evolutionary Morphing. VIS 05 IEEE Visualization. doi: 10.1109/VISUAL.2005.1532826

  • Wilkinson, D. M., & Ruxton, G. D. (2012). Understanding selection for long necks in different taxa. Biological Reviews,87(3), 616–630.

    Article  PubMed  Google Scholar 

  • Zweers, G. A., Vanden Berge, J. C., & Koppendraier, R. (1987). Avian cranio-cervical systems. Part I: Anatomy of the cervical column in the chicken (Gallus gallus L.). Acta Morphologica Neerlando-Scandinavica,25, 131–155.

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Pr Christine Lefèvre for the access of specimens from the collections (Muséum National d’Histoire Naturelle, Paris). They also thank Amandine Blin from the ‘plate-forme de morphométrie’ of the UMS 2700 (CNRS, MNHN) for access to the surface scanner.

Funding

This study was financially supported by the Action transversale du Muséum (ATM) and the Agence National de la Recherche (ANR): Project ID #ANR-16-CE33-0025 (AVINECK), Project Coordinator: A. Abourachid.

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  1. Lea Terray and Olivia Plateau have Equal Authorship.

Authors and Affiliations

  1. UMR 7205 Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National D’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, CP 50, 57 rue Cuvier, 75005, Paris, France

    Léa Terray, Arnaud Delapré & Raphaël Cornette

  2. Faculté des sciences, Département de géosciences, Université de Fribourg, Chemin du musée 6, 1700, Fribourg, Switzerland

    Olivia Plateau

  3. UMR 7179 Mécanismes Adaptatifs Et Evolution (Mecadev), Muséum National d’Histoire Naturelle – CNRS., CP 55, 57 rue Cuvier, 75231, Paris, France

    Anick Abourachid & Christine Böhmer

  4. UMR 6457, SUBATECH, IMT-Atlantique, Université de Nantes, CNRS/IN2P3, 4 rue Alfred Kastler, Nantes, France

    Xavier de la Bernardie

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  1. Léa Terray
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Correspondence to Léa Terray or Olivia Plateau.

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11692_2020_9495_MOESM1_ESM.pdf

Two first axes of the linear discriminant analysis (LDA) performed on cervical vertebrae to visualize the nine modules. The order of vertebrae in the neck is indicated. (PDF 28 kb)

11692_2020_9495_MOESM2_ESM.pdf

Two first axes of the principal component analysis (PCA) performed on cervical vertebrae. The order of vertebrae in the neck is indicated. Points are colored according to modules. Vertebrae belonging to one same neck are linked, forming the shape trajectory of each specie, and the line is colored according to taxa. (PDF 54 kb)

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Terray, L., Plateau, O., Abourachid, A. et al. Modularity of the Neck in Birds (Aves). Evol Biol 47, 97–110 (2020). https://doi.org/10.1007/s11692-020-09495-w

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