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Deciphering the roles of environment and development in the evolution of a Late Triassic assemblage of conodont elements

Published online by Cambridge University Press:  16 May 2019

Pauline Guenser ,
Louise Souquet ,
Sylvain Dolédec ,
Michele Mazza ,
Manuel Rigo  and
Nicolas Goudemand
Pauline Guenser
Affiliation:
Université Lyon, ENS de Lyon, CNRS, Université Claude Bernard Lyon 1, Institut de Génomique Fonctionnelle de Lyon, UMR 5242, 46 Allée d'Italie, F-69364 Lyon Cedex 07, France. E-mail: louise.souquet@ens-lyon.fr, nicolas.goudemand@ens-lyon.fr.
Louise Souquet
Affiliation:
Université Lyon, ENS de Lyon, CNRS, Université Claude Bernard Lyon 1, Institut de Génomique Fonctionnelle de Lyon, UMR 5242, 46 Allée d'Italie, F-69364 Lyon Cedex 07, France. E-mail: louise.souquet@ens-lyon.fr, nicolas.goudemand@ens-lyon.fr.
Sylvain Dolédec
Affiliation:
Université Lyon, CNRS, Université Claude Bernard Lyon 1, Laboratoire d’Écologie des Hydrosystèmes Naturels et Anthropisés, UMR 5023, 3-6 rue Raphaël Dubois–Bâtiments Forel, 69622 Villeurbanne Cedex 43, France. E-mail: sylvain.doledec@univ-lyon1.fr
Michele Mazza
Affiliation:
c/o Dipartimento di Scienze Chimiche e Geologiche, Università degli Studi di Modena e Reggio Emilia, via Campi 103, I-41125 Modena, Italy. E-mail: michele.mza@gmail.com
Manuel Rigo
Affiliation:
IGG-CNR, Via G. Gradenigo 6, 35131 Padova, Italy. E-mail: manuel.rigo@unipd.it
Nicolas Goudemand
Affiliation:
Université Lyon, ENS de Lyon, CNRS, Université Claude Bernard Lyon 1, Institut de Génomique Fonctionnelle de Lyon, UMR 5242, 46 Allée d'Italie, F-69364 Lyon Cedex 07, France. E-mail: louise.souquet@ens-lyon.fr, nicolas.goudemand@ens-lyon.fr.
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Abstract

To assess evolutionary processes in deep time, it is essential to understand the roles of development and environment, both recorded through the morphological variability of fossil assemblages. Thanks to their great abundance and the high temporal resolution of their fossil record, conodont elements are ideal to address this issue. In this paper, we present the first quantitative study of a Carnian–Norian (Late Triassic) assemblage of closely related P1 conodont elements. Using geometric morphometrics (landmarks, sliding landmarks, and elliptic Fourier analysis), we explore the main axes of phenotypic variation and relate them to classically used taxonomic characters. We show that some important taxonomic features follow laws of covariation, hence highlighting developmental constraints. Furthermore, the intraspecific variation within all considered species, either Carnian or Norian forms, is similarly restricted, emphasizing, for the first time in conodont P1 elements, a common line of least resistance to evolution, which means that similar intrinsic (developmental) factors were acting on these taxa and likely biased the evolutionary trajectories of all these taxa in a similar way. Because the evolution between Carnian and Norian forms is known to have followed a trajectory that is significantly different from the line of least resistance, strong extrinsic pressures, such as environmental disturbances, were probably at play around the Carnian/Norian boundary to counteract the effects of these intrinsic, developmental constraints.

Type
Articles
Information
Paleobiology , Volume 45 , Issue 3 , August 2019 , pp. 440 - 457
Copyright
Copyright © The Paleontological Society. All rights reserved 2019 

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Footnotes

*

Present address: Université Lyon, CNRS, Université Claude Bernard Lyon 1, Laboratoire d’Écologie des Hydrosystèmes Naturels et Anthropisés, UMR 5023, 3-6 rue Raphaël Dubois–Bâtiments Forel, 69622 Villeurbanne Cedex 43, France. E-mail: pauline.guenser@univ-lyon1.fr

‡

These authors contributed equally to this work.

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.m48h8ht

References

Literature Cited

Anderson, M. J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26:32–46.Google Scholar
Anderson, M. J. 2017. Permutational multivariate analysis of variance (PERMANOVA). Wiley statsRef: statistics reference online. doi: 10.1002/9781118445112.stat07841.Google Scholar
Anderson, M. J., and Walsh, D. C.. 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecological Monographs 83:557–574.Google Scholar
Balini, M., Bertinelli, A., Di Stefano, P., Guaiumi, C., Levera, M., Mazza, M., Muttoni, G., Nicora, A., Preto, N., and Rigo, M.. 2010. The late Carnian–Rhaetian succession at Pizzo Mondello (Sicani Mountains). Albertiana 39:36–57.Google Scholar
Barnett, S. G. 1972. The evolution of Spathognathodus remscheidensis in New York, New Jersey, Nevada, and Czechoslovakia. Journal of Paleontology 46:900–917.Google Scholar
Benton, M. J., Forth, J., and Langer, M. C.. 2014. Models for the rise of the dinosaurs. Current Biology 24:R87–R95.Google Scholar
Blanc, L., Chessel, D., and Dolédec, S.. 1998. Etude de la stabilité temporelle des structures spatiales par analyses d'une série de tableaux de relevés faunistiques totalement appariés. Bulletin Français de la Pêche et de la Pisciculture 348:1–21.Google Scholar
Bonhomme, V., Picq, S., Gaucherel, C., Claude, J.. 2014. Momocs: outline analysis using R. Journal of Statistical Software 56:1–24.Google Scholar
Chen, J., Beatty, T. W., Henderson, C. M., and Rowe, H.. 2009. Conodont biostratigraphy across the Permian–Triassic boundary at the Dawen section, Great Bank of Guizhou, Guizhou Province, South China: implications for the Late Permian extinction and correlation with Meishan. Journal of Asian Earth Sciences 36:442–458.Google Scholar
Chen, Y., Neubauer, T. A., Krystyn, L., and Richoz, S.. 2016. Allometry in Anisian (Middle Triassic) segminiplanate conodonts and its implications for conodont taxonomy. Palaeontology 59:725–741.Google Scholar
Ciampaglio, C. N. 2002. Determining the role that ecological and developmental constraints play in controlling disparity: examples from the crinoid and blastozoan fossil record. Evolution and Development 4:170–188.Google Scholar
Condamine, F. L., Rolland, J., and Morlon, H.. 2013. Macroevolutionary perspectives to environmental change. Ecology Letters 16:72–85.Google Scholar
Croll, V. M., Aldridge, R. J., and Harvey, P. K.. 1982. Computer applications in conodont taxonomy: characterization of blade elements. Miscellaneous paper. Geological Society of London, Computer Applications in Geology I & II 14:237–246.Google Scholar
Donoghue, P. C. 1998. Growth and patterning in the conodont skeleton. Philosophical Transactions of the Royal Society of London B 353:633–666.Google Scholar
Donoghue, P. C., and Purnell, M. A.. 1999. Growth, function, and the conodont fossil record. Geology 27:251–254.Google Scholar
Donoghue, P. C., Forey, P. L., and Aldridge, R. J.. 2000. Conodont affinity and chordate phylogeny. Biological Reviews 75:191–251.Google Scholar
Dray, S., Dufour, A. B., and Chessel, D.. 2007. The ade4 package-II: two-table and K-table methods. R News 7:47–52.Google Scholar
Epstein, A. G., Epstein, J. B., and Harris, L. D.. 1977. Conodont color alteration: an index to organic metamorphism. Geological Survey Professional Paper 995. U.S. Governmet Printing Office, Washington, D.C.Google Scholar
Erlich, A., Moulton, D. E., Goriely, A., and Chirat, R.. 2016. Morphomechanics and developmental constraints in the evolution of ammonites shell form. Journal of Experimental Zoology B 326:437–450.Google Scholar
Erwin, D. H. 2017. Developmental push or environmental pull? The causes of macroevolutionary dynamics. History and Philosophy of the Life Sciences 39:36.Google Scholar
Fletcher, B. J., Brentnall, S. J., Anderson, C. W., Berner, R. A., and Beerling, D. J.. 2008. Atmospheric carbon dioxide linked with Mesozoic and early Cenozoic climate change. Nature Geoscience 1:43.Google Scholar
Girard, C., and Renaud, S.. 2007. Quantitative conodont-based approaches for correlation of the Late Devonian Kellwasser anoxic events. Palaeogeography, Palaeoclimatology, Palaeoecology 250:114–125.Google Scholar
Girard, C., and Renaud, S.. 2008. Disentangling allometry and response to Kellwasser anoxic events in the Late Devonian conodont genus Ancyrodella. Lethaia 41:383–394.Google Scholar
Girard, C., and Renaud, S.. 2011. The species concept in a long-extinct fossil group, the conodonts. Comptes Rendus Palevol 10:107–115.Google Scholar
Girard, C., Renaud, S., and Korn, D.. 2004a. Step-wise morphological trends in fluctuating environments: evidence in the Late Devonian conodont genus Palmatolepis. Geobios 37:404–415.Google Scholar
Girard, C., Renaud, S., and Sérayet, A.. 2004b. Morphological variation of Palmatolepis Devonian conodonts: species versus genus. Comptes Rendus Palevol 3:1–8.Google Scholar
Goudemand, N., Orchard, M. J., Urdy, S., Bucher, H., and Tafforeau, P.. 2011. Synchrotron-aided reconstruction of the conodont feeding apparatus and implications for the mouth of the first vertebrates. Proceedings of the National Academy of Sciences USA 108:8720–8724.Google Scholar
Hallam, A. 1996. Major bio-events in the Triassic and Jurassic. Pp. 265–283 in Walliser, O. H., ed. Global events and event stratigraphy in the Phanerozoic. Springer, Berlin.Google Scholar
Hammer, Ø., Harper, D. A. T., and Ryan, P. D.. 2001. Paleontological statistics software: package for education and data analysis. Palaeontologia Electronica 4:9.Google Scholar
Hayashi, S. 1968. The Permian conodonts in chert of the Adoyama Formation, Ashio mountains, central Japan. Earth Science 22:63–77.Google Scholar
Hunt, G. 2007. Evolutionary divergence in directions of high phenotypic variance in the ostracode genus Poseidonamicus. Evolution 61:1560–1576.Google Scholar
Huxley, J. 1942. Evolution: the modern synthesis. George Allen and Unwin, London.Google Scholar
Jablonski, D. 2017. Approaches to macroevolution: 1. General concepts and origin of variation. Evolutionary Biology 44:427–450.Google Scholar
Joachimski, M. M., Pancost, R. D., Freeman, K. H., Ostertag-Henning, C., and Buggisch, W.. 2002. Carbon isotope geochemistry of the Frasnian–Famennian transition. Palaeogeography, Palaeoclimatology, Palaeoecology 181:91–109.Google Scholar
Joachimski, M. M., von Bitter, P. H., and Buggisch, W.. 2006. Constraints on Pennsylvanian glacioeustatic sea-level changes using oxygen isotopes of conodont apatite. Geology 34:277–280.Google Scholar
Jones, D. 2009. Directional evolution in the conodont Pterospathodus. Paleobiology 35:413–431.Google Scholar
Jones, D., Purnell, M. A., and von Bitter, P. H.. 2009. Morphological criteria for recognising homology in isolated skeletal elements: comparison of traditional and morphometric approaches in conodonts. Palaeontology 52:1243–1256.Google Scholar
Kent, D. V., Olsen, P. E., and Muttoni, G.. 2017. Astrochronostratigraphic polarity time scale (APTS) for the Late Triassic and Early Jurassic from continental sediments and correlation with standard marine stages. Earth-Science Reviews 166:153–180.Google Scholar
Klapper, G., and Foster, C. T. Jr. 1993. Shape analysis of Frasnian species of the Late Devonian conodont genus Palmatolepis. Paleontological Society Memoir 32. Journal of Paleontology 67:1–35.Google Scholar
Kozur, H. 1972. Die Conodontengattung Metapolygnathus (Hayashi, 1968) und ihr stratigraphischer Wert (Conodont genus Metapolygnathus (Hayashi, 1968) and their stratigraphic values). Institut für Geologie und Paläontologie, Münster, Germany. [In German.]Google Scholar
Kuhl, F. P., and Giardina, C. R.. 1982. Elliptic Fourier features of a closed contour. Computer Graphics and Image Processing 18:236–258.Google Scholar
Lavit, C., Escoufier, Y., Sabatier, R., and Traissac, P.. 1994. The ACT (STATIS method). Computational Statistics & Data Analysis 18:97–119.Google Scholar
Levins, R., and Lewontin, R. C.. 1985. The dialectical biologist. Harvard University Press, Cambridge.Google Scholar
Martínez-Pérez, C., Plasencia, P., Jones, D., Kolar-Jurkovšek, T., Sha, J., Botella, H., and Donoghue, P. C.. 2014a. There is no general model for occlusal kinematics in conodonts. Lethaia 47:547–555.Google Scholar
Martínez-Pérez, C., Rayfield, E. J., Purnell, M. A., and Donoghue, P. C.. 2014b. Finite element, occlusal, microwear and microstructural analyses indicate that conodont microstructure is adapted to dental function. Palaeontology 57:1059–1066.Google Scholar
Martínez-Pérez, C., Purnell, M. A., Rayfield, E., and Donoghue, P. C. J.. 2016. Shedding light into the function of the earliest vertebrate skeleton. EGU General Assembly Conference Abstracts 18:17108.Google Scholar
Mayr, E. 1982. Speciation and macroevolution. Evolution 36:1119–1132.Google Scholar
Mazza, M., and Martínez-Pérez, C.. 2015. Unravelling conodont (Conodonta) ontogenetic processes in the Late Triassic through growth series reconstructions and X-ray microtomography. Bollettino della Società Paleontologica Italiana 54:161–186.Google Scholar
Mazza, M., and Martínez-Pérez, C.. 2016. Evolutionary convergence in conodonts revealed by synchrotron-based tomographic microscopy. Palaeontologia Electronica 19:1–11.Google Scholar
Mazza, M., Furin, S., Spötl, C., and Rigo, M.. 2010. Generic turnovers of Carnian/Norian conodonts: climatic control or competition? Palaeogeography, Palaeoclimatology, Palaeoecology 290:120–137.Google Scholar
Mazza, M., Rigo, M., and Nicora, A.. 2011. A new Metapolygnathus platform conodont species and its implications for Upper Carnian global correlations. Acta Palaeontologica Polonica 56:121–131.Google Scholar
Mazza, M., Cau, A., and Rigo, M.. 2012a. Application of numerical cladistic analyses to the Carnian–Norian conodonts: a new approach for phylogenetic interpretations. Journal of Systematic Palaeontology 10:401–422.Google Scholar
Mazza, M., Rigo, M., and Gullo, M.. 2012b. Taxonomy and biostratigraphic record of the Upper Triassic conodonts of the Pizzo Mondello section (western Sicily, Italy), GSSP candidate for the base of the Norian. Rivista Italiana di Paleontologia e Stratigrafia 118:85–130.Google Scholar
Mazza, M., Nicora, A., and Rigo, M.. 2018. Metapolygnathus parvus Kozur, 1972 (Conodonta): a potential primary marker for the Norian GSSP (Upper Triassic). Bollettino della Società Paleontologica Italiana 57:81–101.Google Scholar
Mock, R. 1979. Gondolella carpathica n. sp., eine wichtige tuvalische Conodontenart. Geologisch-Paläontologische Mitteilungen Innsbruck 9:171–174.Google Scholar
Moix, P., Kozur, H. W., Stampfli, G. M., and Mostler, H.. 2007. New paleontological, biostratigraphical and paleogeographic results from the Triassic of the Mersin Mélange, SE Turkey. The global Triassic. New Mexico Museum of Natural History Science Bulletin 41:282–311.Google Scholar
Mosher, L. C. 1968. Evolution of Triassic platform conodonts. Journal of Paleontology 42:947–954.Google Scholar
Moulton, D. E., Goriely, A., and Chirat, R.. 2012. Mechanical growth and morphogenesis of seashells. Journal of Theoretical Biology 311:69–79.Google Scholar
Murdock, D. J., Sansom, I. J., and Donoghue, P. C.. 2013. Cutting the first “teeth”: a new approach to functional analysis of conodont elements. Proceedings of the Royal Society of London B 280:20131524.Google Scholar
Murphy, M. A., and Cebecioglu, M. K.. 1984. The Icriodus steinachensis and I. claudiae lineages (Devonian conodonts). Journal of Paleontology 58:1399–1411.Google Scholar
Murphy, M. A., and Springer, K. B.. 1989. Morphometric study of the platform elements of Amydrotaxis praejohnsoni n. sp. (Lower Devonian, Conodonts, Nevada). Journal of Paleontology 63:349–355.Google Scholar
Muttoni, G., Kent, D. V., Olsen, P. E., Di Stefano, P., Lowrie, W., Bernasconi, S. M., and Hernández, F. M.. 2004. Tethyan magnetostratigraphy from Pizzo Mondello (Sicily) and correlation to the Late Triassic Newark astrochronological polarity time scale. Geological Society of America Bulletin 116:1043–1058.Google Scholar
Nicora, A., Balini, M., Bellanca, A., Bertinelli, A., Bowring, S. A., Di Stefano, P., Dumitrica, P., et al. 2007. The Carnian/Norian boundary interval at Pizzo Mondello (Sicani Mountains, Sicily) and its bearing for the definition of the GSSP of the Norian Stage. Albertiana 36:102–129.Google Scholar
Noyan, Ö. F., and Kozur, H. W.. 2007. Revision of the late Carnian–early Norian conodonts from the Stefanion section (Argolis, Greece) and their palaeobiogeographic implications. Neues Jahrbuch für Geologie und Paläontologie-Abhandlungen 245:159–178.Google Scholar
Onoue, T., Zonneveld, J.-P., Orchard, M. J., Yamashita, M., Yamashita, K., Sato, H, and Kusaka, S.. 2016. Paleoenvironmental changes across the Carnian/Norian boundary in the Black Bear Ridge section, British Columbia, Canada. Palaeogeography, Palaeoclimatology, Palaeoecology 441:721–733.Google Scholar
Orchard, M. J. 1991. Upper Triassic conodont biochronology and new index species from the Canadian Cordillera. Bulletin of the Geological Survey of Canada 417:299–335.Google Scholar
Orchard, M. J. 2013. Five new genera of conodonts from the Carnian–Norian boundary beds of Black Bear Ridge, northeast British Columbia, Canada. The Triassic system. New Mexico Museum of Natural History and Science Bulletin 61:445–457.Google Scholar
Orchard, M. J.. 2014. Conodonts from the Carnian–Norian boundary (Upper Triassic) of Black Bear Ridge, Northeastern British Columbia. New Mexico Museum of Natural History and Science 64:1–139.Google Scholar
Pálfy, J., Demény, A., Haas, J., Carter, E. S., Görög, Á., Halász, D., Oravecz-Scheffer, A., Hetényi, M., Márton, E., and Orchard, M. J.. 2007. Triassic–Jurassic boundary events inferred from integrated stratigraphy of the Csövár section, Hungary. Palaeogeography, Palaeoclimatology, Palaeoecology 244:11–33.Google Scholar
Payne, J. L., and Van de Schootbrugge, B.. 2007. Life in Triassic oceans: links between planktonic and benthic recovery and radiation. Pp. 165–189 in Evolution of primary producers in the sea. Elsevier, San Diego, Calif.Google Scholar
Purnell, M. A. 1994. Skeletal ontogeny and feeding mechanisms in conodonts. Lethaia 27:129–138.Google Scholar
Purnell, M. A., Donoghue, P. C., and Aldridge, R. J.. 2000. Orientation and anatomical notation in conodonts. Journal of Paleontology 74:113–122.Google Scholar
R Core Team. 2018. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Renaud, S., and Girard, C.. 1999. Strategies of survival during extreme environmental perturbations: evolution of conodonts in response to the Kellwasser crisis (Upper Devonian). Palaeogeography, Palaeoclimatology, Palaeoecology 146:19–32.Google Scholar
Renaud, S., Auffray, J.-C., and Michaux, J.. 2006. Conserved phenotypic variation patterns, evolution along lines of least resistance, and departure due to selection in fossil rodents. Evolution 60:1701–1717.Google Scholar
Rigo, M., and Joachimski, M. M.. 2010. Palaeoecology of Late Triassic conodonts: constraints from oxygen isotopes in biogenic apatite. Acta Palaeontologica Polonica 55:471–479.Google Scholar
Rigo, M., Preto, N., Roghi, G., Tateo, F., and Mietto, P.. 2007. A rise in the carbonate compensation depth of western Tethys in the Carnian (Late Triassic): deep-water evidence for the Carnian Pluvial Event. Palaeogeography, Palaeoclimatology, Palaeoecology 246:188–205.Google Scholar
Rigo, M., Trotter, J. A., Preto, N., and Williams, I. S.. 2012. Oxygen isotopic evidence for Late Triassic monsoonal upwelling in the northwestern Tethys. Geology 40:515–518.Google Scholar
Rigo, M., Mazza, M., Karádi, V., and Nicora, A.. 2018. New Upper Triassic conodont biozonation of the Tethyan realm. Pp. 189–235 in Tanner, L., ed. The Late Triassic world. Springer, Cham.Google Scholar
Ritter, S. M. 1989. Morphometric patterns in Middle Triassic Neogondolella mombergensis (Conodonta), Fossil Hill, Nevada. Journal of Paleontology 63:233–245.Google Scholar
Robert, P., and Escoufier, Y.. 1976. A unifying tool for linear multivariate statistical methods: the RV-coefficient. Applied Statistics:257–265.Google Scholar
Roghi, G., Mirro, P., and Vecchia, F. M. Dalla. 1995. Contribution to the conodont biostratigraphy of the Dolomia di Forni (Upper Triassic, Carnian, NE Italy). Memorie di Scienze Geologische Universita di Padova 47:125–133.Google Scholar
Roghi, G., Gianolla, P., Minarelli, L., Pilati, C., and Preto, N.. 2010. Palynological correlation of Carnian humid pulses throughout western Tethys. Palaeogeography, Palaeoclimatology, Palaeoecology 290:89–106.Google Scholar
Rohlf, F. J. 2006. tpsDig, Version 2.10. Department of Ecology and Evolution, State University of New York, Stony Brook, NY.Google Scholar
Rohlf, F. J. 2007. tpsRelw, Version 1.45. Department of Ecology and Evolution, State University of New York, Stony Brook, NY.Google Scholar
Rohlf, F. J., and Marcus, L. F.. 1993. A revolution morphometrics. Trends in Ecology and Evolution 8:129–132.Google Scholar
Schluter, D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50:1766–1774.Google Scholar
Siahsarvie, R. 2012. Comparaison de la divergence morphologique et génétique chez la souris domestique au cours de son expansion géographique. Ph.D. thesis. Université Montpellier 2. 56 p.Google Scholar
Simms, M. J., and Ruffell, A. H.. 1990. Climatic and biotic change in the late Triassic. Journal of the Geological Society 147:321–327.Google Scholar
Stanley, G. D. Jr. 1988. The history of early Mesozoic reef communities: a three-step process. Palaios 3:170–183.Google Scholar
Sun, Y., Joachimski, M. M., Wignall, P. B., Yan, C., Chen, Y., Jiang, H., Wang, L., and Lai, X.. 2012. Lethally hot temperatures during the Early Triassic greenhouse. Science 338:366–370.Google Scholar
Thioulouse, J., and Chessel, D.. 1987. Les analyses multitableaux en écologie factorielle. I: De la typologie d’état à la typologie de fonctionnement par l'analyse triadique. Acta Oecologica Oecologia Generalis 8:463–480.Google Scholar
Tolmacheva, T., and Löfgren, A.. 2000. Morphology and paleogeography of the Ordovician conodont Paracordylodus gracilis Lindström, 1955: comparison of two populations. Journal of Paleontology 74:1114–1121.Google Scholar
Trotter, J. A., Williams, I. S., Barnes, C. R., Lécuyer, C., and Nicoll, R. S.. 2008. Did cooling oceans trigger Ordovician biodiversification? Evidence from conodont thermometry. Science 321:550–554.Google Scholar
Trotter, J. A., Williams, I. S., Nicora, A., Mazza, M., and Rigo, M.. 2015. Long-term cycles of Triassic climate change: a new δ18O record from conodont apatite. Earth and Planetary Science Letters 415:165–174.Google Scholar
Urdy, S., Wilson, L. A., Haug, J. T., and Sánchez-Villagra, M. R.. 2013. On the unique perspective of paleontology in the study of developmental evolution and biases. Biological Theory 8:293–311.Google Scholar
Wainwright, P. C. 2007. Functional versus morphological diversity in macroevolution. Annual Review of Ecology, Evolution, and Systematics 38:381–401.Google Scholar
Wenzel, B., Lécuyer, C., and Joachimski, M. M.. 2000. Comparing calcite and phosphate oxygen isotope paleothermometers—δ18O of Silurian brachiopods and conodonts. Geochimica et Cosmochimica Acta 64:1859–1872.Google Scholar
Wickham, H. 2016. Ggplot2: elegant graphics for data analysis. Springer, New York.Google Scholar
Wright, S. 1982. The shifting balance theory and macroevolution. Annual Review of Genetics 16:1–20.Google Scholar