Morphological integration and modularity in the hyperkinetic feeding system of aquatic-foraging snakes.
Functional modularity
Procrustes superimposition
morphological evolution
morphometrics
skull
snakes
Journal
Evolution; international journal of organic evolution
ISSN: 1558-5646
Titre abrégé: Evolution
Pays: United States
ID NLM: 0373224
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
11
09
2020
revised:
05
11
2020
accepted:
13
11
2020
pubmed:
24
11
2020
medline:
5
10
2021
entrez:
23
11
2020
Statut:
ppublish
Résumé
The kinetic skull is a key innovation that allowed snakes to capture, manipulate, and swallow prey exclusively using their heads using the coordinated movement of eight bones. Despite these unique feeding behaviors, patterns of evolutionary integration and modularity within the feeding bones of snakes in a phylogenetic framework have yet to be addressed. Here, we use a dataset of 60 μCT-scanned skulls and high-density geometric morphometric methods to address the origin and patterns of variation and integration in the feeding bones of aquatic-foraging snakes. By comparing alternate superimposition protocols allowing us to analyze the entire kinetic feeding system simultaneously, we find that the feeding bones are highly integrated, driven predominantly by functional selective pressures. The most supported pattern of modularity contains four modules, each associated with distinct functional roles: the mandible, the palatopterygoid arch, the maxilla, and the suspensorium. Further, the morphological disparity of each bone is not linked to its magnitude of integration, indicating that integration within the feeding system does not strongly constrain morphological evolution, and that adequate biomechanical solutions to a wide range of feeding ecologies and behaviors are readily evolvable within the constraint due to integration in the snake feeding system.
Banques de données
Dryad
['10.5061/dryad.rbnzs7h9m']
Types de publication
Comparative Study
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
56-72Informations de copyright
© 2020 The Authors. Evolution © 2020 The Society for the Study of Evolution.
Références
Adams, D. C. 1999. Methods for shape analysis of landmark data from articulated structures. Evol. Ecol. Res. 1:959-970.
Adams, D. C. 2004. Character displacement via aggressive interference in Appalachian salamanders. Ecology 85:2664-2670.
Adams, D. C. 2014. A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Syst. Biol. 63:685-697.
Adams, D. C. 2016. Evaluating modularity in morphometric data: challenges with the RV coefficient and a new test measure. Methods Ecol. Evol. 7:565-572.
Adams, D. C., and E. Otárola-Castillo. 2013. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4:393-399.
Adams, D. C., and F. J. Rohlf. 2000. Ecological character displacement in Plethodon: biomechanical differences found from a geometric morphometric study. Proc. Natl. Acad. Sci. 97:4106-4111.
Adams, D. C., and M. L. Collyer. 2016. On the comparison of the strength of morphological integration across morphometric datasets. Evolution 70:2623-2631.
Adams, D. C., and M. L. Collyer. 2018. Multivariate phylogenetic comparative methods: evaluations, comparisons, and recommendations. Syst. Biol. 67:14-31.
Adams, D. C., and M. L. Collyer. 2019. Comparing the strength of modular signal, and evaluating alternative modular hypotheses, using covariance ratio effect sizes with morphometric data. Evolution 73:2352-2367.
Adams, D. C., and R. N. Felice. 2014. Assessing trait covariation and morphological integration on phylogenies using evolutionary covariance matrices. PLoS One 9:e94335.
Adams, D. C., F. J. Rohlf, and D. E. Slice. 2004. Geometric morphometrics: ten years of progress following the ‘revolution’. Ital. J. Zool. 71:5-16.
Adams, D. C., F. J. Rohlf, and D. E. Slice. 2013. A field comes of age: geometric morphometrics in the 21st century. Hystrix 24:7.
Andjelković, M., L. Tomović, and A. Ivanović. 2016. Variation in skull size and shape of two snake species (Natrix natrixand Natrix tessellata). Zoomorphology 135:243-253.
Andjelković, M., L. Tomović, and A. Ivanović. 2017. Morphological integration of the kinetic skull in Natrix snakes. J. Zool. 303:188-198.
Atchley, W. R., and B. K. Hall. 1991. A model for development and evolution of complex morphological structures. Biol. Rev. 66:101-157.
Arlegi, M., C. Veschambre-Couture, and A. Gómez-Olivencia. 2020. Evolutionary selection and morphological integration in the vertebral column of modern humans. Am. J. Phys. Anthropol. 171:17-36.
Bardua, C., R. N. Felice, A. Watanabe, A. C. Fabre, and A. Goswami. 2019a. A practical guide to sliding and surface semilandmarks in morphometric analyses. Integr. Comp. Biol. 1:obz016.
Bardua, C., M. Wilkinson, D. J. Gower, E. Sherratt, and A. Goswami. 2019b. Morphological evolution and modularity of the caecilian skull. BMC Evol. Biol. 19:30.
Bardua, C., A. C. Fabre, M. Bon, K. Das, E. L. Stanley, D. C. Blackburn, and A. Goswami. 2020. Evolutionary integration of the frog cranium. Evolution 74:1200-1215.
Bell, E., B. Andres, and A. Goswami. 2011. Integration and dissociation of limb elements in flying vertebrates: a comparison of pterosaurs, birds and bats. J. Evol. Biol. 24:2586-2599.
Boltt, R. E., and R. F. Ewer. 1964. The functional anatomy of the head of the puff adder, Bitis arietans (Merr.). J. Morphol. 114:83-105.
Bon, M., C. Bardua, A. Goswami, and A. C. Fabre. 2020. Cranial integration in the fire salamander, Salamandra salamandra (Caudata: Salamandridae). Biol. J. Linn. Soc. 130:178-194.
Boughner, J. C., M. Buchtová, K. Fu, V. Diewert, B. Hallgrímsson, and J. M. Richman. 2007. Embryonic development of Python sebae-I: staging criteria and macroscopic skeletal morphogenesis of the head and limbs. Zoology 110:212-230.
Caldwell, M. W. 2019. The origin of snakes: morphology and the fossil record. Pp. 1-326. CRC Press, Boca Raton, FL. https://doi.org/10.1201/9781315118819.
Cheverud, J. M. 1984. Quantitative genetics and developmental constraints on evolution by selection. J. Theor. Biol. 110:155-171.
Cheverud, J. M. 1996. Developmental integration and the evolution of pleiotropy. Am. Zool. 36:44-50.
Collyer, M. L., M. A. Davis, and D. C. Adams. 2020. Making heads or tails of combined landmark configurations in geometric morphometric data. Evol. Biol. 47:193-204.
Cundall, D. 1983. Activity of head muscles during feeding by snakes: a comparative study. Am. Zool. 23:383-396.
Cundall, D., and H. W. Greene. 2000. Feeding in snakes. Feeding. Pp. 293-333 in K. Schwenk, ed. Academic Press, Amsterdam, the Netherlands. https://doi.org/10.1016/B978-012632590-4/50010-1.
Davis, M. A., M. R. Douglas, M. L. Collyer, and M. E. Douglas. 2016. Deconstructing a species-complex: geometric morphometric and molecular analyses define species in the Western Rattlesnake (Crotalus viridis). PLoS One 11:e0146166.
Deufel, A., and D. Cundall. 2003. Feeding in Atractaspis (Serpentes: Atractaspididae): a study in conflicting functional constraints. Zoology 106:43-61.
dos Santos, M. M., F. M. da Silva, E. Hingst-Zaher, F. A. Machado, H. E. D. Zaher, and A. L. da Costa Prudente. 2017. Cranial adaptations for feeding on snails in species of Sibynomorphus (Dipsadidae: Dipsadinae). Zoology 120:24-30.
Dumont, M., C. E. Wall, L. Botton-Divet, A. Goswami, S. Peigné, and A. C. Fabre. 2016. Do functional demands associated with locomotor habitat, diet, and activity pattern drive skull shape evolution in musteloid carnivorans? Biol. J. Linn. Soc. 117:858-878.
Esquerré, D., E. Sherratt, and J. S. Keogh. 2017. Evolution of extreme ontogenetic allometric diversity and heterochrony in pythons, a clade of giant and dwarf snakes. Evolution 71:2829-2844.
Fabre, A. C., D. Bickford, M. Segall, and A. Herrel. 2016. The impact of diet, habitat use, and behaviour on head shape evolution in homalopsid snakes. Biol. J. Linn. Soc. 118:634-647.
Fabre, A. C., C. Bardua, M. Bon, J. Clavel, R. N. Felice, J. W. Streicher, J. Bonnel, E. L. Stanley, D. C. Blackburn, and A. Goswami. 2020. Metamorphosis shapes cranial diversity and rate of evolution in salamanders. Nat. Ecol. Evol. 4:1129-1140.
Felice, R. N., and A. Goswami. 2018. Developmental origins of mosaic evolution in the avian cranium. Proc. Natl. Acad. Sci. 115:555-560.
Felice, R. N., M. Randau, and A. Goswami. 2018. A fly in a tube: macroevolutionary expectations for integrated phenotypes. Evolution 72:2580-2594.
Felice, R. N., A. Watanabe, A. R. Cuff, E. Noirault, D. Pol, L. M. Witmer, M. A. Norell, P. M. O'Connor, and A. Goswami. 2019. Evolutionary integration and modularity in the archosaur cranium. Integr. Comp. Biol. 59:371-382.
Goswami, A. 2006. Cranial modularity shifts during mammalian evolution. Am. Nat. 168:270-280.
Goswami, A., and P. D. Polly. 2010a. Methods for studying morphological integration and modularity. Paleontol. Soc. Pap. 16:213-243.
Goswami, A., and P. D. Polly. 2010b. The influence of modularity on cranial morphological disparity in Carnivora and Primates (Mammalia). PLoS One 5:e9517.
Goswami, A., J. B. Smaers, C. Soligo, and P. D. Polly. 2014. The macroevolutionary consequences of phenotypic integration: from development to deep time. Philos. Trans. R. Soc. 369:20130254.
Goswami, A., A. Watanabe, R. N. Felice, C. Bardua, A. C. Fabre, and P. D. Polly. 2019. High-density morphometric analysis of shape and integration: the good, the bad, and the not-really-a-problem. Integr. Comp. Biol. 59:669-683.
Gunz, P., P. Mitteroecker, and F. L. Bookstein. 2005. Semilandmarks in Three Dimensions. Modern Morphometrics in Physical Anthropology. Pp. 73-98 in D. E. Slice, ed. Developments in Primatology: Progress and Prospects. Springer, Boston, MA. https://doi.org/10.1007/0-387-27614-9_3.
Gunz, P., and P. Mitteroecker. 2013. Semilandmarks: a method for quantifying curves and surfaces. Hystrix 24:103-109.
Hallgrímsson, B., K. Willmore, and B. K. Hall. 2002. Canalization, developmental stability, and morphological integration in primate limbs. Am. J. Phys. Anthropol. 119:131-158.
Hallgrímsson, B., H. Jamniczky, N. M. Young, C. Rolian, T. E. Parsons, J. C. Boughner, and R. S. Marcucio. 2009. Deciphering the palimpsest: studying the relationship between morphological integration and phenotypic covariation. Evol. Biol. 36:355-376.
Hampton, P. M. 2011. Comparison of cranial form and function in association with diet in natricine snakes. J. Morphol. 272:1435-1443.
Jackson, K. 2003. The evolution of venom-delivery systems in snakes. Zool. J. Linn. Soc. 137:337-354.
Jayne, B. C., H. K. Voris, and P. K. L. Ng. 2002. Snake circumvents constraints on prey size. Nature 418:143-143.
Jayne, B. C., H. K. Voris, and P. K. L. Ng. 2018. How big is too big? Using crustacean-eating snakes (Homalopsidae) to test how anatomy and behaviour affect prey size and feeding performance. Biol. J. Linn. Soc. 123:636-650.
Johnston, P. 2014. Homology of the jaw muscles in lizards and snakes-a solution from a comparative gnathostome approach. Anat. Rec. 297:574-585.
Jones, K. E., L. Benitez, K. D. Angielczyk, and S. E. Pierce. 2018. Adaptation and constraint in the evolution of the mammalian backbone. BMC Evol. Biol. 18:1-13.
Jones, K. E., S. Gonzalez, K. D. Angielczyk, and S. E. Pierce. 2020. Regionalization of the axial skeleton predates functional adaptation in the forerunners of mammals. Nat. Ecol. Evol. 4:470-478.
Kardong, K. V. 1977. Kinesis of the jaw apparatus during swallowing in the cottonmouth snake, Agkistrodon piscivorus. Copeia 1977:338-348.
Kardong, K. V. 1979. ‘Protovipers’ and the evolution of snake fangs. Evolution 33:433-443.
Khannoon, E. R., and S. E. Evans. 2015. The development of the skull of the Egyptian cobra Naja h. haje (Squamata: Serpentes: Elapidae). PLoS One 10:e0122185.
Klaczko, J., E. Sherratt, and E. Z. Setz. 2016. Are diet preferences associated to skulls shape diversification in xenodontine snakes? PLoS One 11:e0148375.
Klingenberg, C. P. 2008. Morphological integration and developmental modularity. Annu. Rev. Ecol. Evol. Syst. 39:115-132.
Klingenberg, C. P. 2014. Studying morphological integration and modularity at multiple levels: concepts and analysis. Philos. Trans. R. Soc. 369:20130249.
Kojima, Y., I. Fukuyama, T. Kurita, M. Y. B. Hossman, and K. Nishikawa. 2020. Mandibular sawing in a snail-eating snake. Sci. Rep. 10:1-5.
Lebrun, R., and M. J. Orliac. 2017. MorphoMuseuM: an online platform for publication and storage of virtual specimens. Paleontol. Soc. Pap. 22:183-195.
Martín-Serra, A., B. Figueirido, and P. Palmqvist. 2020. Changing modular patterns in the carnivoran pelvic girdle. J. Mamm. Evol. 27:237-243.
Marshall, A. F., C. Bardua, D. J. Gower, M. Wilkinson, E. Sherratt, and A. Goswami. 2019. High-density three-dimensional morphometric analyses support conserved static (intraspecific) modularity in caecilian (Amphibia: Gymnophiona) crania. Biol. J. Linn. Soc. 126:721-742.
Melo, D., A. Porto, J. M. Cheverud, and G. Marroig. 2016. Modularity: genes, development, and evolution. Annu. Rev. Ecol. Evol. Syst. 47:463-486.
Murphy, J. C. 2012. Marine invasions by non-sea snakes, with thoughts on terrestrial-aquatic-marine transitions. Integr. Comp. Biol. 52:217-226.
Mushinsky, H. R., J. J. Hebrard, and D. S. Vodopich. 1982. Ontogeny of water snake foraging ecology. Ecology 63:1624-1629.
Murta-Fonseca, R. A., A. Machado, R. T. Lopes, and D. S. Fernandes. 2019. Sexual dimorphism in Xenodon neuwiediiskull revealed by geometric morphometrics (Serpentes; Dipsadidae). Amphibia-Reptilia 40:461-474.
Moon, B. R., D. A. Penning, M. Segall, and A. Herrel. 2019. Feeding in Snakes: form, function, and evolution of the feeding system. Pp. 527-574 in V. Belsand I. Whishaw, eds. Feeding in vertebrates. Springer, Cham, Switzerland.
Mori, A., and S. E. Vincent. 2008. An integrative approach to specialization: relationships among feeding morphology, mechanics, behaviour, performance and diet in two syntopic snakes. J. Zool. 275:47-56.
Navalón, G., J. Marugán-Lobón, J. A. Bright, C. R. Cooney, and E. J. Rayfield. 2020. The consequences of craniofacial integration for the adaptive radiations of Darwin's finches and Hawaiian honeycreepers. Nat. Ecol. Evol. 4:270-278.
Olson, E. C., and R. L. Miller. 1958. Morphological integration. Pp. 1-376. University of Chicago Press, Chicago.
Palci, A., M. S. Lee, and M. N. Hutchinson. 2016. Patterns of postnatal ontogeny of the skull and lower jaw of snakes as revealed by micro-CT scan data and three-dimensional geometric morphometrics. J. Anat. 229:723-754.
Palci, A., M. W. Caldwell, M. N. Hutchinson, T. Konishi, and M. S. Lee. 2020. The morphological diversity of the quadrate bone in squamate reptiles as revealed by high-resolution computed tomography and geometric morphometrics. J. Anat. 236:210-227.
Pavlicev, M., J. M. Cheverud, and G. P. Wagner. 2009. Measuring morphological integration using eigenvalue variance. Evol. Biol. 36:157-170.
Polachowski, K. M., and I. Werneburg. 2013. Late embryos and bony skull development in Bothropoides jararaca (Serpentes, Viperidae). Zoology 116:36-63.
Pyron, R. A., and F. T. Burbrink. 2014. Early origin of viviparity and multiple reversions to oviparity in squamate reptiles. Ecol. Lett. 17:13-21.
Raff, R. A. 1996. The shape of life: genes, development, and the evolution of animal form. Pp. 1-544. University of Chicago Press, Chicago.
Randau, M., and A. Goswami. 2017a. Unravelling intravertebral integration, modularity and disparity in Felidae (Mammalia). Evol. Dev. 19:85-95.
Randau, M., and A. Goswami. 2017b. Morphological modularity in the vertebral column of Felidae (Mammalia, Carnivora). BMC Evol. Biol. 17:133.
Randau, M., and A. Goswami. 2018. Shape covariation (or the lack thereof) between vertebrae and other skeletal traits in felids: the whole is not always greater than the sum of parts. Evol. Biol. 45:196-210.
Revell, L. J. 2009. Size-correction and principal components for interspecific comparative studies. Evolution 63:3258-3268.
Rohlf, F. J., and D. Slice. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Syst. Biol. 39:40-59.
Rohlf, F. J., and M. Corti. 2000. Use of two-block partial least-squares to study covariation in shape. Syst. Biol. 49:740-753.
Savitzky, A. H. 1983. Coadapted character complexes among snakes: fossoriality, piscivory, and durophagy. Am. Zool. 23:397-409.
Scanferla, A. 2016. Postnatal ontogeny and the evolution of macrostomy in snakes. R. Soc. Open Sci. 3:160612.
Schlager, S. 2017. Morpho and Rvcg-shape analysis in R: R-packages for geometric morphometrics, shape analysis and surface manipulations. Pp. 217-256 in G. Zheng, S. Li, and G. Székely, eds. Statistical shape and deformation analysis. Academic Press, Cambridge, MA.
Sherratt, E., K. L. Sanders, A. Watson, M. N. Hutchinson, M. S. Lee, and A. Palci. 2019. Heterochronic shifts mediate ecomorphological convergence in skull shape of microcephalic sea snakes. Integr. Comp. Biol. 59:616-624.
Segall, M., R. Cornette, A. C. Fabre, R. Godoy-Diana, and A. Herrel. 2016. Does aquatic foraging impact head shape evolution in snakes? Proc. R. Soc. 283:20161645.
Segall, M., A. Herrel, and R. Godoy-Diana. 2019. Hydrodynamics of frontal striking in aquatic snakes: drag, added mass, and the possible consequences for prey capture success. Bioinspiration & Biomimetics. 14(3):036005. https://doi.org/10.1088/1748-3190/ab0316.
Segall, M., R. Cornette, R. Godoy-Diana, and A. Herrel. 2020. Exploring the functional meaning of head shape disparity in aquatic snakes. Ecol. Evol. 10:6993-7005.
Sheverdyukova, H. V. 2019. Development of the Osteocranium in Natrix natrix (Serpentes, Colubridae) Embryogenesis II: development of the jaws, palatal complex and associated bones. Acta Zool. 100:282-291.
Silva, F. M., A. L. D. C. Prudente, F. A. Machado, M. M. Santos, H. Zaher, and E. Hingst-Zaher. 2018. Aquatic adaptations in a Neotropical coral snake: a study of morphological convergence. J. Zoolog. Syst. Evol. 56:382-394.
Souto, N. M., R. A. Murta-Fonseca, A. S. Machado, R. T. Lopes, and D. S. Fernandes. 2019. Snakes as a model for measuring skull preparation errors in geometric morphometrics. J. Zool. 309:12-21.
Uetz, P., S. Cherikh, G. Shea, I. Ineich, P. D. Campbell, I. V. Doronin, J. Rosado, A. Wynn, K. Tighe, R. Mcdiarmid, et al. 2019. A global catalog of primary reptile type specimens. Zootaxa 4695:438-450.
Vidal-García, M., and J. S. Keogh. 2017. Phylogenetic conservatism in skulls and evolutionary lability in limbs-morphological evolution across an ancient frog radiation is shaped by diet, locomotion and burrowing. BMC Evol. Biol. 17:1-15.
Vidal-García, M., L. Bandara, and J. S. Keogh. 2018. ShapeRotator: an R tool for standardized rigid rotations of articulated three-dimensional structures with application for geometric morphometrics. Ecol. Evol. 8:4669-4675.
Vincent, S. E., B. R. Moon, A. Herrel, and N. J. Kley. 2007. Are ontogenetic shifts in diet linked to shifts in feeding mechanics? Scaling of the feeding apparatus in the banded watersnake Nerodia fasciata. J. Exp. Biol. 210:2057-2069.
Wagner, G. P., and L. Altenberg. 1996. Perspective: complex adaptations and the evolution of evolvability. Evolution 50:967-976.
Wagner, G. P., M. Pavlicev, and J. M. Cheverud. 2007. The road to modularity. Nat. Rev. Genet. 8:921-931.
Wainwright, P. C., and B. A. Richard. 1995. Predicting patterns of prey use from morphology of fishes. Environ. Biol. Fishes 44:97-113.
Watanabe, A., A. C. Fabre, R. N. Felice, J. A. Maisano, J. Müller, A. Herrel, and A. Goswami. 2019. Ecomorphological diversification in squamates from conserved pattern of cranial integration. Proc. Natl. Acad. Sci. 116:14688-14697.
Werneburg, I., K. M. Polachowski, and M. N. Hutchinson. 2015. Bony skull development in the Argus monitor (Squamata, Varanidae, Varanus panoptes) with comments on developmental timing and adult anatomy. Zoology 118:255-280.
Wiley, D. F., N. Amenta, D. A. Alcantara, D. Ghosh, Y. J. Kil, E. Delson, W. Harcourt-Smith, F. J. Rohlf, K. St John, et al. 2005. Evolutionary morphing. Pp. 431-438 in Proceedings of IEEE Visualization 2005 (VIS’05). IEEE, Minneapolis, MN.