Hostname: page-component-745bb68f8f-l4dxg Total loading time: 0 Render date: 2025-01-23T14:44:19.780Z Has data issue: false hasContentIssue false
  • English
  • Français

Is 3D, a more accurate quantitative method than 2D, crucial for analyzing disparity patterns in extinct marine arthropods (Trilobita)?

Published online by Cambridge University Press:  21 January 2025

Catherine Crônier Open the ORCID record for Catherine Crônier [Opens in a new window] ,
Sébastien Couette Open the ORCID record for Sébastien Couette [Opens in a new window]  and
Rémi Laffont Open the ORCID record for Rémi Laffont [Opens in a new window]
Catherine Crônier*
Affiliation:
Université de Lille, CNRS, UMR 8198–Evo-Eco-Paleo, F-59000 Lille, France
Sébastien Couette
Affiliation:
Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 21000 Dijon, France EPHE, PSL University, 21000 Dijon, France
Rémi Laffont
Affiliation:
Biogéosciences, UMR CNRS 6282, Université de Bourgogne, 21000 Dijon, France
*
Corresponding author: Catherine Crônier; Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Phacopid trilobites are well documented during the Paleozoic. Nevertheless, while 2D quantitative analyses have advanced our understanding of the morphological relationships among trilobites, the quantification of their morphological traits in 3D remains rarely documented. Based on two sets of morphological data (head and tail), 2D versus 3D shape quantification approaches were used to explore shape allometries as well as to explore how the shape variations can be explained by the phylogenetic relationships among phacopid trilobite species for the first time. We demonstrate that (1) there are similar patterns of morphological variability across taxa in 3D and 2D; (2) there are rather congruent results between 3D and 2D to discriminate taxa; (3) 2D and 3D landmarks capture different levels of detail, and the third dimension in 3D is very important for making taxonomic distinctions at the genus level; (4) there is congruity between 2D and 3D datasets for allometric patterns with results showing similar allometric slopes among species exhibiting a glabellar length decrease during growth leading to wider cephala; (5) the phylomorphospaces show tree branches that do not intersect, suggesting possible phylogenetic constraints on morphospace occupation for each species and supporting the idea that the Austerops and Morocops groups are sister clades that experienced different modes of morphological evolution; and (6) the morphological descriptors in morphometric analyses in 2D and 3D throughout phacopid evolution are effective.

Type
Article
Information
Paleobiology , First View , pp. 1 - 19
Check for updates
Copyright
Copyright © The Author(s), 2025. Published by Cambridge University Press on behalf of Paleontological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Adams, D. C. 2014. A generalized K statistic for estimating phylogenetic signal from shape and other high-dimensional multivariate data. Systematic Biology 63:685–697.CrossRefGoogle ScholarPubMed
Adams, D. C., and Nistri, A.. 2010. Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evolutionary Biology 10:216.CrossRefGoogle ScholarPubMed
Adams, D. C., and Otarola-Castillo, E.. 2013. Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution 4:393–399.CrossRefGoogle Scholar
Adams, D. C., Rohlf, F. J., and Slice, D. E.. 2004. Geometric morphometrics: ten years of progress following the “revolution.” Italian Journal of Zoology 71:5–16.CrossRefGoogle Scholar
Adams, D. C., Rohlf, F. J., and Slice, D. E.. 2013. A field comes of age: geometric morphometrics in the 21st century. Hystrix 24:7–14.Google Scholar
Adrain, J. M., Westrop, S., Chatterton, B., and Ramsköld, L.. 2000. Silurian trilobite alpha diversity and the end-Ordovician mass extinction. Paleobiology 26:625–646.2.0.CO;2>CrossRefGoogle Scholar
Alberti, G. K. B. 1970. Trilobiten des jüngeren Siluriums sowie des Unter- und Mitteldevons. II. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 525:1–233.Google Scholar
Álvarez, A., and Perez, S. I.. 2013. Two- versus three-dimensional morphometric approaches in macroevolution: insight from the mandible of caviomorph rodents. Evolutionary Biology 40:150–157.CrossRefGoogle Scholar
Andrialovanirina, N., Caillault, É. P., Couette, S., Laffont, R., Poloni, L., Lutet-Toti, C., and Mahé, K.. 2023. Asymmetry of sagittal otolith shape based on inner ear side tested on Mediterranean Red Mullet (Mullus barbatus Linnaeus, 1758): comparative analysis of 2D and 3D otolith shape data. Symmetry 15:1067.CrossRefGoogle Scholar
Arthur, W. 2002. The interaction between developmental bias and natural selection: from centipede segments to a general hypothesis. Heredity 89:239–246.CrossRefGoogle ScholarPubMed
Basse, M. 2006. Eifel-Trilobiten IV. Proetida (3), Phacopida (3). Goldschneck, Quelle & Meyer Verlag, Wiebelsheim.Google Scholar
Bault, V., Balseiro, D., Monnet, C., and Crônier, C.. 2022a. Post-Ordovician trilobite diversity and evolutionary faunas. Earth-Science Reviews 230:104035.CrossRefGoogle Scholar
Bault, V., Crônier, C., and Monnet, C.. 2022b. Morphological disparity trends in Devonian trilobites from North Africa. Palaeontology 65:e12623.CrossRefGoogle Scholar
Berssenbrugge, P., Berlin, N. F., Kebeck, G., Runte, C., Jung, S., Kleinheinz, J., and Dirksen, D.. 2014. 2D and 3D analysis methods of facial asymmetry in comparison. Journal of Cranio-Maxillofacial Surgery 42:e327–e334.CrossRefGoogle ScholarPubMed
Blomberg, S. P., Garland, T., and Ives, A. R.. 2003. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745.Google ScholarPubMed
Bookstein, F. L. 1991. Morphometric tools for landmark data. Cambridge University Press, Cambridge.Google Scholar
Buser, T. J., Sidlauskas, B. L., and Summers, A. P.. 2018. 2D or not 2D? Testing the utility of 2D vs. 3D landmark data in geometric morphometrics of the Sculpin subfamily Oligocottinae (Pisces; Cottoidea). Anatomical Record 301:806–818.CrossRefGoogle ScholarPubMed
Cardini, A. 2014. Missing the third dimension in geometric morphometrics: how to assess if 2D images really are a good proxy for 3D structures? Hystrix 25:73–81.Google Scholar
Cardini, A. 2016. Lost in the other half: improving accuracy in geometric morphometric analyses of one side of bilaterally symmetric structures. Systematic Biology 65:1096–1106.CrossRefGoogle ScholarPubMed
Cardini, A. 2017. Left, right or both? Estimating and improving accuracy of one-side-only geometric morphometric analyses of cranial variation. Journal of Zoological Systematics and Evolutionary Research 55:1–10.CrossRefGoogle Scholar
Cardini, A., and Chiapelli, M.. 2020. How flat can a horse be? Exploring 2D approximations of 3D crania in equids. Zoology 139:125746.CrossRefGoogle ScholarPubMed
Cardini, A., de Jong, Y. A., and Butynski, T. M.. 2022. Can morphotaxa be assessed with photographs? Estimating the accuracy of two-dimensional cranial geometric morphometrics for the study of threatened populations of African monkeys. Anatomical Record 305:1402–1434.CrossRefGoogle Scholar
Chatterton, B. D. E., Fortey, R. A., Brett, S., Gibb, K., and Kellar, R. M.. 2006. Trilobites from the upper Lower to Middle Devonian Timrhanrhart Formation, JbelGara el Zguilma, southern Morocco. Palaeontographica Canadiana 24:1–177.Google Scholar
Collyer, M. L., and Adams, D. C.. 2018. RRPP: an R package for fitting linear models to high-dimensional data using residual randomization. Methods in Ecology and Evolution 9:1772–1779.CrossRefGoogle Scholar
Crônier, C. 2013. Morphological disparity and developmental patterning: contribution of phacopid trilobites. Palaeontology 56:1263–1271.CrossRefGoogle Scholar
Crônier, C., and Clarkson, E. N. K.. 2001. Variation of eye-lens distribution in a new late Devonian phacopids trilobite. Transactions of the Royal Society of Edinburgh (Earth Sciences) 92:103–113.CrossRefGoogle Scholar
Crônier, C., and Courville, P.. 2003. Variations du rythme du développement chez les trilobites Phacopidae néodévoniens. Comptes Rendus Palevol 2:577–585.CrossRefGoogle Scholar
Crônier, C., Renaud, S., Feist, R., and Auffray, J.-C.. 1998. Ontogeny of Trimerocephalus lelievrei (Trilobita, Phacopida) in relation to paedomorphosis: a morphometric approach. Paleobiology 24:359–370.Google Scholar
Crônier, C., Feist, R., and Auffray, J.-C.. 2004. Variation in the eye of Acuticryphops (Phacopina, Trilobita) and its evolutionary significance: a biometric and morphometric approach. Paleobiology 30:470–480.2.0.CO;2>CrossRefGoogle Scholar
Crônier, C., Auffray, J.-C., and Courville, P.. 2005. A quantitative comparison of the ontogeny of two closely-related Upper Devonian phacopid trilobites. Lethaia 38:123–135.CrossRefGoogle Scholar
Crônier, C., Budil, P., Fatka, O., and Laibl, L.. 2015. Intraspecific bimodal variability in eye lenses of two Devonian trilobites. Paleobiology 41:554–569.CrossRefGoogle Scholar
Dornburg, A., Sidlauskas, B., Santini, F., Sorenson, L., Near, T. J., and Alfaro, M.E.. 2011. The influence of an innovative locomotor strategy on the phenotypic diversification of triggerfish (Family: Balistidae). Evolution 65:1912–1926.CrossRefGoogle ScholarPubMed
Dryden, I. L., and Mardia, K. V.. 1998. Statistical shape analysis. Wiley Series in Probability and Statistics. Wiley, Chichester, U.K.Google Scholar
Eldredge, N. 1972. Systematics and evolution of Phacops rana (Green, 1832) and Phacops iowensis Delo, 1935 (Trilobita) from the Middle Devonian of North America. Bulletin of the American Museum of Natural History 147:45–114.Google Scholar
Eldredge, N. 1973. Systematics of Lower and Lower Middle Devonian species of the trilobite Phacops Emmrich in North America. Bulletin of the American Museum Natural History 151:285–338.Google Scholar
Elewa, A. M. T. 2004. Application of geometric morphometrics to the study of shape polymorphism in Eocene ostracodes from Egypt and Spain. Pp. 7–28 in Elewa, A.M.T., ed. Morphometrics: applications in biology and paleontology. Springer-Verlag, Berlin.CrossRefGoogle Scholar
Erwin, D. H. 2007. Disparity: morphological pattern and developmental context. Palaeontology 50:57–73.CrossRefGoogle Scholar
Esteve, J., Rubio, P., Zamora, S., and Rahman, I. A.. 2017. Modelling enrolment in Cambrian trilobites. Palaeontology 60:423–432.CrossRefGoogle Scholar
Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1–15.CrossRefGoogle Scholar
Foote, M. 1991. Morphologic patterns of diversification: examples from trilobites. Palaeontology 34:461–485.Google Scholar
Fortey, R. A., and Owens, R. M.. 1999. Feeding habits in trilobites. Palaeontology 42:429–465.CrossRefGoogle Scholar
Gómez, J. M., Gonzáles-Megías, A., Narbona, E., Navarro, L., Perfectti, F., and Armas, C.. 2021. Phenotypic plasticity guides Moricandia arvensis divergence and convergence across the Brassicaceae floral morphospace. New Phytologist 233:1479–1493.CrossRefGoogle ScholarPubMed
Goswami, A., Binder, W. J., Meachen, J., and O'Keefe, F. R.. 2015. The fossil record of phenotypic integration and modularity: a deep-time perspective on developmental and evolutionary dynamics. Proceedings of the National Academy of Science USA 12:4891–4896.CrossRefGoogle Scholar
Gould, S. J. 1977. Ontogeny and phylogeny. Belknap Press of Harvard University Press, Cambridge, Mass.Google Scholar
Gould, S. J. 2002. The structure of evolutionary theory. Belknap Press of Harvard University Press, Cambridge, Mass.Google Scholar
Hallgrimsson, B., Percival, C. J., Green, R., Young, N. M., Mio, W., and Marcusio, R.. 2015. Morphometrics, 3D imaging, and craniofacial development. Current Topics in Developmental Biology 115:561–597.CrossRefGoogle ScholarPubMed
Hawle, I., and Corda, A. J. C.. 1847. Prodom einer Monographie der böhmischen Trilobiten. J.G. Calve'sche Buchhandlung, Prague.Google Scholar
Hicks, H. 1873. On the Tremadoc rocks in the neighbourhood of St. David's, Pembrokeshire, with special reference to those of the Arenig and Llandeilo groups and their fossil contents. Quarterly Journal of the Geological Society of London 29:39–52.CrossRefGoogle Scholar
Hopkins, M. J. 2013. Decoupling of taxonomic diversity and morphological disparity during decline of the Cambrian trilobite family Pterocephaliidae. Journal of Evolutionary Biology 26:1665–1676.CrossRefGoogle ScholarPubMed
Hopkins, M. J., and Pearson, J. K.. 2016. Non-linear ontogenetic shape change in Cryptolithus tesselatus (Trilobita) using three-dimensional geometric morphometrics. Palaeontologica Electronica 19.3(42A):1–54.Google Scholar
Hughes, N.C. 2003. Trilobite body patterning and the evolution of arthropod tagmosis. BioEssays 25:386–395.CrossRefGoogle ScholarPubMed
Jacobs, G. S., and Carlucci, J. R.. 2019. Ontogeny and shape change of the phacopid trilobite Calyptaulax. Journal of Paleontology 93:1105–1125.CrossRefGoogle Scholar
Khaldi, A. Y., Crônier, C., Hainaut, G., Abbache, A., and Ouali Mehadji, A.. 2016. A trilobite faunule from the Lower Devonian of the Saoura Valley, Algeria: biodiversity, morphological variability and palaeobiogeographical affinities. Geological Magazine 153:357–387.CrossRefGoogle Scholar
Kim, K., Sheets, H. D., Haney, R. A., and Mitchell, C. E.. 2002. Morphometric analysis of ontogeny and allometry of the Middle Ordovician trilobite Triarthrus becki. Paleobiology 28:364–377.2.0.CO;2>CrossRefGoogle Scholar
Kimmel, C. B., Small, C. M., and Knope, M. L.. 2017. A rich diversity of opercle bone shape among teleost fishes. PLoS ONE 12:e0188888.CrossRefGoogle ScholarPubMed
Klingenberg, C. P., and Gidaszewski, N. A.. 2010. Testing and quantifying phylogenetic signals and homoplasy in morphometric data. Systematic Biology 59:245–261.CrossRefGoogle ScholarPubMed
Klingenberg, C. P., and McIntyre, G. S.. 1998. Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with Procrustes methods. Evolution 52:1363–1375.CrossRefGoogle ScholarPubMed
Klingenberg, C. P., Barluenga, M., and Meyer, A.. 2002. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56:1909–1920.Google ScholarPubMed
Legendre, P., and Legendre, L.. 2012. Numerical ecology, 3rd edition. Elsevier, Amsterdam.Google Scholar
Le Maître, D. 1952. La faune du Dévonien inférieur et moyen de la Saoura et des abords de l'Erg el Djemel (Sud oranais). Mémoire de la Carte géologique de l'Algérie 12:1–170.Google Scholar
Maia, R., Rubenstein, D. R., and Shawkey, M. D.. 2013. Key ornamental innovations facilitate diversification in an avian radiation. Proceedings of the National Academy of Sciences USA 110:10687–10692.CrossRefGoogle Scholar
Månsson, K., and Clarkson, E. N. K.. 2012. Ontogeny of the Upper Cambrian (Furongian) Olenid trilobite Protopeltura aciculate (Angelin, 1854) from Skåne and Västergötland, Sweden. Palaeontology 55:887–901.CrossRefGoogle Scholar
Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer Research 27:209–200.Google Scholar
McKellar, R. C., and Chatterton, B. D. E.. 2009. Early and Middle Devonian Phacopidae (Trilobita) of southern Morocco. Palaeontographica Canadiana 28:1–110.Google Scholar
McWhinnie, K. C., and Parsons, K. J.. 2019. Shaping up? A direct comparison between 2D and low cost 3D shape analysis using African cichlid mandibles. Environmental Biology of Fishes 102:927–938.CrossRefGoogle Scholar
Mitteroecker, P., and Gunz, P.. 2009. Advances in Geometric Morphometrics. Evolutionary Biology 36:235–247.CrossRefGoogle Scholar
Mitteroecker, P., and Schaefer, K.. 2022. Thirty years of geometric morphometrics: achievements, challenges, and the ongoing quest for biological meaningfulness. Yearbook of Biological Anthropology 178:181–210.CrossRefGoogle ScholarPubMed
Munkemuller, T., Lavergne, S., Bzeznik, B., Dray, S., Jombart, T., Schiffers, K., and Thuiller, W.. 2012. How to measure and test phylogenetic signal. Methods in Ecology and Evolution 3:743–756.CrossRefGoogle Scholar
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., et al. 2018. Vegan: community ecology package, R package version 2.5-3. https://CRAN.R-project.org/package=vegan (accessed 2018).Google Scholar
Oudot, M., Crônier, C., Neige, P., and Holloway, D.. 2018. Phylogeny of some Devonian trilobites based on morphological characters and consequences to the systematics of Austerops (Phacopidae). Journal of Systematic Palaeontology 17:775–790.CrossRefGoogle Scholar
Oudot, M., Neige, P., Laffont, R., Navarro, N., Khaldi, A. Y., and Crônier, C.. 2019. Functional integration for enrolment constrains evolutionary variation of phacopid trilobites despite developmental modularity. Palaeontology 62:805–821.CrossRefGoogle Scholar
Přibyl, A., Vaněk, J., and Pek, I.. 1985. Phylogeny and taxonomy of family Cheiruridae (Trilobita). Acta Universitatis Palackianae Olomucensis Facultas Rerum Naturalium Geographica-Geologica 83:107–193.Google Scholar
Raymond, P. E. 1913. Subclass Trilobita. Pp. 692–729 in Eastman, C. R., ed. Textbook of palaeontology, 2nd ed. MacMillan Company, New York.Google Scholar
R Development Core Team. 2019. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Revell, L. J., Harmon, L. J., and Collar, D. C.. 2008. Phylogenetic signal, evolutionary process, and rate. Systematic Biology 57:591–601.CrossRefGoogle ScholarPubMed
Rohlf, F. J. 2015. The tps series of software. Hystrix 26:9–12.Google Scholar
Rohlf, F. J., and Marcus, L. F.. 1993. A revolution morphometrics. Trends in Ecology and Evolution 8:129–132.CrossRefGoogle Scholar
Sadler, P. M. 1974. Trilobites from the Gorran Quartzites, Ordovician of South Cornwall. Palaeontology 17:71–93.Google Scholar
Sakamoto, M., and Ruta, M.. 2012. Convergence and divergence in the evolution of cat skulls: temporal and spatial patterns of morphological diversity. PLoS ONE 7:e39752.CrossRefGoogle ScholarPubMed
Saleh, F., Guenser, P., Gibert, C., Balseiro, D., Serra, F., Waisfeld, B. G., Antcliffe, J. B., et al. 2022. Contrasting Early Ordovician assembly patterns highlight the complex initial stages of the Ordovician radiation. Scientific Reports 12:3852.CrossRefGoogle ScholarPubMed
Santos, B. F., Perrard, A., and Brady, S. G.. 2019. Running in circles in phylomorphospace: host environment constrains morphological diversification in parasitic wasps. Proceedings of the Royal Society B 286:10182352.Google ScholarPubMed
Shaw, A. B. 1957. Quantitative trilobite studies II. Measurement of the dorsal shell of non-agnostidean trilobites. Journal of Paleontology 31:193–207.Google Scholar
Sherratt, E., Serb, J. M., and Adams, D. C.. 2017. Rates of morphological evolution, asymmetry and morphological integration of shell shape in scallops. BMC Evolutionary Biology 17:248.CrossRefGoogle ScholarPubMed
Sidlauskas, B. 2008. Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach. Evolution 62:3135–3156.CrossRefGoogle ScholarPubMed
Slater, G. J., Price, S. A., Santini, F., and Alfaro, M. E.. 2010. Diversity versus disparity and the radiation of modern cetaceans. Proceedings of the Royal Society B 277:3097–3104.CrossRefGoogle ScholarPubMed
Smith, L. H., and Lieberman, B. S.. 1999. Disparity and constraint in olenelloid trilobites and the Cambrian radiation. Paleobiology 25:459–470.CrossRefGoogle Scholar
Sundberg, F. A. 1996. Morphological diversification of Ptychopariida (Trilobita) from the Marjumiid Biomere (Middle and Upper Cambrian). Paleobiology 22:49–65.CrossRefGoogle Scholar
Swiderski, D. L. 1993. Morphological evolution of the scapula in tree squirrels, chipmunks, and ground squirrels (Sciuridae): an analysis using thin-plate splines. Evolution 47:1854–1873.CrossRefGoogle ScholarPubMed
Webster, M. 2007. A Cambrian peak in morphological variation within trilobite species. Science 317:499–502.CrossRefGoogle ScholarPubMed
Yoder, J. B., Clancey, E., Des Roches, S., Eastman, J. M., Gentry, L., Godsoe, W., Hagey, T. J., et al. 2010. Ecological opportunity and the origin of adaptive radiations. Journal of Evolutionary Biology 23:1581–1596.CrossRefGoogle ScholarPubMed
Zelditch, M. L., Bookstein, F. L., and Lundrigan, B. L.. 1992. Ontogeny of integrated skull growth in the cotton rat Sigmodon fulviventer. Evolution 46:1164–1180.CrossRefGoogle ScholarPubMed