Abstract
In the context of geometric morphometric analyses of modularity and integration using Procrustes methods, some researchers have recently claimed that “high-density geometric morphometric data exceed the traditional landmark-based methods in the characterization of morphology and allow more nuanced comparisons across disparate taxa” and also that, using “high-density” data (i.e., with dozens or hundreds of semilandmarks), “potential issues [with tests of modularity and integration] are unlikely to obscure genuine biological signal”. I show that the first claim is invalidly tautological and, therefore, flawed, while the second one is a speculation. “High-density” geometric morphometrics is a potentially useful tool for the quantification of continuous morphological variation in evolutionary biology, but cannot be said to represent absolute accuracy, simply because more measurements increase information, but do not by default imply that this information is accurate. Semilandmarks are an analytical expedient to break the continuity of regions devoid of clearly corresponding landmarks, but the shape variables which they generate are a function of the specific choice of the placement and possible mathematical manipulation of these points. Not only there are infinite ways of splitting a curve or surface into discrete points, but also none of the methods to slide the semilandmarks increases the accuracy of their mapping onto the underlying biological homology: indeed, none of them is based on a biological model, and the assumption of universal equivalence between geometric and biological correspondence is unverified, if at all verifiable. Besides, in the specific context of modularity and integration using Procrustes geometric morphometrics, the limited number of scenarios simulated until now may provide interesting clues, but do not yet allow strong statements and clear generalizations. The Procrustes superimposition does alter the ‘true’ covariance structure of the data and sliding semilandmarks further contributes to this change. Although we hope that this might only add a negligible source of inaccuracy, and simulations using landmarks (but no semilandmarks yet) suggest that this might be the case, it is too early to confidently share the view, expressed by the promoters of high-density methods, that this is “Not-Really-a-Problem”. The evidence is very preliminary and the dichotomy may not be this simple, with the magnitude (from negligible to large) and direction (inflation of modularity, integration, or both) of a potential bias in the tests likely to vary in ways specific to the data being analysed. We need more studies that provide robust and generalizable evidence, without indulging in invalid tautology and over-interpretation. With both landmarks and semilandmarks, what is measured should be functional to the specific hypothesis and we should be clear on where the treatment of the data is pure mathematics and where there is a biological model that supports the maths.
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Notes
As a referee remarked “In many studies that use dense correspondences the aim is simple identification, which … does not require points to be equivalent in any biologically meaningful sense (because differences are not interpreted).[However,] how we measure affects relative differences among specimens in complex ways—arbitrary measurements give arbitrary distances … [which] may not tally with the everyday experience of many workers, especially in computer science, and increasingly in biology, where the seeking of dense correspondences between surfaces of objects by algorithm is common”.
In fact, a reviewer argued that, even if most of the time the ‘noise’ might be relatively more important in microevolutionary studies, where the ‘signal’ tends to be smaller, there might be interesting exceptions: “Microevolutionary differences tend to be small. That said, depending on the shapes of the objects, the problem could be bigger in macroevolutionary studies if one takes the simulations in G19 at face value: large differences in points that are far from the center of the object—for example, tips of bird beaks—will strongly affect the position of the centroid and, therefore, the artifactual covariance introduced by Procrustes. That effect will be even more pronounced if the beak has more surface area than the cranium and semilandmarks are placed with equal density in both regions”.
(i.e., the likely stronger covariance between contiguous landmarks, such as those within a ‘module’).
References
Adams DC, Cardini A, Monteiro LR et al (2011) Morphometrics and phylogenetics: Principal components of shape from cranial modules are neither appropriate nor effective cladistic characters. J Hum Evol 60:240–243
Adams DC, Collyer ML, Kaliontzopoulou A, Sherratt E (2017) Geomorph: Software for geometric morphometric analyses. R package version 3.0.5. https://cran.r-project.org/package=geomorph
Adams DC, Rohlf FJ, Slice DE (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. Italian J Zool 71:5–16
Adams DC, Rohlf FJ, Slice DE (2013) A field comes of age: geometric morphometrics in the 21st century. Hystrix Italian J Mammals 24:7–14
Bookstein FL (2017) A newly noticed formula enforces fundamental limits on geometric morphometric analyses. Evol Biol 44:522–541. https://doi.org/10.1007/s11692-017-9424-9
Bookstein FL (2015) Integration, disintegration, and self-similarity: characterizing the scales of shape variation in landmark data. Evol Biol 42:395–426. https://doi.org/10.1007/s11692-015-9317-8
Cardini A (2019) Integration and modularity in procrustes shape data: is there a risk of spurious results? Evol Biol. https://doi.org/10.1007/s11692-018-9463-x
Cardini A, Loy A (2013) On growth and form in the computer era: from geometric to biological morphometrics. Hystrix Italian J Mammal 24:1–5. https://doi.org/10.4404/hystrix-24.1-8749
Cardini A, O’Higgins P, Rohlf FJ (2019) Seeing distinct groups where there are none: spurious patterns from between-group PCA. Evol Biol 46:303–316. https://doi.org/10.1007/s11692-019-09487-5
DeQuardo J, Bookstein FL, Green WDK et al (1996) Spatial relationships of neuroanatomic landmarks in schizophrenia. Psychiatry Res Neuroimag 67:81–95. https://doi.org/10.1016/0925-4927(96)02733-3
Felsenstein J (2004) Inferring Phylogenies. Sunderland, Massachusetts, Sinauer Associates, Incorporated
Ferretti A, Cardini A, Crampton JS et al (2013) Rings without a lord? Enigmatic fossils from the lower Palaeozoic of Bohemia and the Carnic Alps. Lethaia 46:211–222. https://doi.org/10.1111/let.12004
Goswami A, Watanabe A, Felice RN et al (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. https://doi.org/10.1093/icb/icz120
Gunz P, Mitteroecker P (2013) Semilandmarks: a method for quantifying curves and surfaces. Hystrix Italian J Mammal 24:103–109
Gunz P, Mitteroecker P, Bookstein FL (2005) Semilandmarks in Three Dimensions. In: Slice DE (ed) Modern morphometrics in physical anthropology. Kluwer Academic Publishers-Plenum Publishers, New York, pp 73–98
Gunz P, Mitteroecker P, Neubauer S et al (2009) Principles for the virtual reconstruction of hominin crania. J Hum Evol 57:48–62. https://doi.org/10.1016/j.jhevol.2009.04.004
Kendall MG, Buckland WR, Institute IS (1957) A dictionary of statistical terms. Published for the International Statistical Institute by Oliver and Boyd
Klingenberg CP (2008) Novelty and “Homology-free” Morphometrics: What’s in a Name? Evol Biol 35:186–190. https://doi.org/10.1007/s11692-008-9029-4
Klingenberg CP (2013) Visualizations in geometric morphometrics: how to read and how to make graphs showing shape changes. Hystrix Italian J Mammal 24:15–24
Klingenberg CP (2016) Size, shape, and form: concepts of allometry in geometric morphometrics. Dev Genes Evol 226:113–137. https://doi.org/10.1007/s00427-016-0539-2
Kovarovic K, Aiello LC, Cardini A, Lockwood CA (2011) Discriminant function analyses in archaeology: are classification rates too good to be true? J Archaeol Sci 38:3006–3018. https://doi.org/10.1016/j.jas.2011.06.028
de León MSP, Zollikofer CPE (2001) Neanderthal cranial ontogeny and its implications for late hominid diversity. Nature 412:534–538. https://doi.org/10.1038/35087573
McCane B (2013) Shape variation in outline shapes. Syst Biol 62:134–146. https://doi.org/10.1093/sysbio/sys080
Navarro N, Maga AM (2016) Does 3D phenotyping yield substantial insights in the genetics of the mouse mandible shape? G3 Genes Genomes Genetics 6:1153–1163. https://doi.org/10.1534/g3.115.024372
O’Higgins P (1997) Methodological issues in the description of forms. Fourier descriptors and their applications in biology. In: Lestrel P (ed) Fourier Descriptors and their Applications in Biology, Cambridge University Press, Cambridge, pp. 74–105 https://doi.org/10.1017/CBO9780511529870.005
O’Higgins P, Cobb SN, Fitton LC et al (2011) Combining geometric morphometrics and functional simulation: an emerging toolkit for virtual functional analyses. J Anat 218:3–15. https://doi.org/10.1111/j.1469-7580.2010.01301.x
Paul OP (2000) The study of morphological variation in the hominid fossil record: biology, landmarks and geometry. J Anat 197:103–120
Oxnard C, O’Higgins P (2009) Biology clearly needs morphometrics. Does morphometrics need biology? Biol Theory 4:84–97. https://doi.org/10.1162/biot.2009.4.1.84
Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy. Front Zool 7:16. https://doi.org/10.1186/1742-9994-7-16
Perez SI, Bernal V, Gonzalez PN (2006) Differences between sliding semilandmark methods in geometric morphometrics, with an application to human craniofacial and dental variation. J Anat 208:769–784. https://doi.org/10.1111/j.1469-7580.2006.00576.x
Polly P (2017) Morphometries and evolution: the challenge of crossing rugged phenotypic landscapes with straight paths. Vavilov J Genetics Breeding 21:452–461
Polly PD (2008a) Developmental dynamics and G-Matrices: can morphometric spaces be used to model phenotypic evolution? Evol Biol 35:83. https://doi.org/10.1007/s11692-008-9020-0
Polly PD (2008b) Adaptive zones and the pinniped ankle: a three-dimensional quantitative analysis of carnivoran tarsal evolution. In: Sargis EJ, Dagosto M (eds) Mammalian evolutionary morphology. Springer, Netherlands, pp 167–196
Rohlf FJ (2000a) On the use of shape spaces to compare morphometric methods. Hystrix Italian J Mammal 11:1–17. https://doi.org/10.4404/hystrix-11.1-4134
Rohlf FJ (2000b) Statistical power comparisons among alternative morphometric methods. Am J Phys Anthropol 111:463–478
Rohlf FJ (1998) On applications of geometric morphometrics to studies of ontogeny and phylogeny. Syst Biol 47:147–158
Rohlf FJ, Marcus LF (1993) A revolution morphometrics. Trends Ecol Evol 8:129–132
Rohlf FJ, Slice D (1990) Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Zool 39:40–59. https://doi.org/10.2307/2992207
Schlager S, Rüdell A (2015) Analysis of the human osseous nasal shape—population differences and sexual dimorphism. Am J Phys Anthropol 157:571–581. https://doi.org/10.1002/ajpa.22749
Schlick-Steiner BC, Steiner FM, Seifert B et al (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annu Rev Entomol 55:421–438
Slice DE (1994) GRF-ND: Generalized rotational fitting of n-dimensional landmark data. Free software. Department of ecology and evolution, State University of New York, Stony Brook, New York, USA
Smith GR (1990) Homology in morphometrics and phylogenetics. In: Proceedings of the Michigan morphometrics workshop. University of Michigan Museum of Zoology, Ann Arbor, pp 325–338
Sokal RR, Sneath PHA (1963) Numerical taxonomy. The principles and practice of numerical classification. Freeman WH, San Francisco
Viscosi V, Cardini A (2011) Leaf morphology, taxonomy and geometric morphometrics: A simplified protocol for beginners. e25630
Watanabe A (2018) How many landmarks are enough to characterize shape and size variation? PLoS ONE 13:e0198341. https://doi.org/10.1371/journal.pone.0198341
Acknowledgements
I am very much in debt to David Polly for the stimulating discussions which we always have had and also for his wonderful review of this paper. A few other scientists could have been as balanced and positive as he was: his supportive comments are the best acknowledgement I could hope for. If David’s task, as an author of G19, was particularly challenging, I did not give for granted that also the second referee was equally positive. For this, I sincerely thank Paul O’Higgins, who also made a great number of useful comments and who, most importantly, first taught me to pay a lot of attention to the implication of the mathematical treatment of landmarks and semilandmarks. We may disagree on whether content is more important than form, but I am in debt to Ulrike Muller for her most helpful replies to my informal initial inquires on a possible response to the paper of G19. If Integrative and Comparative Biology, where G19 is published, was the obvious place to first explore the possibility of a comment, I am very happy that my paper will be out in Zoomorphology, a journal I have strong ties with and one that over the years has become a main venue for morphometric studies. Thus, for the excellent (as usual!) editorial work, I thank a lot both Andreas Schmidt-Rhaesa and Carmelo Fruciano. Finally, I am most grateful to a number of morphometricians and evolutionary biologists who, over the years, have provided feedback (and a good deal of arguing!) on some of the problems I discuss in this paper, and especially to Sandro Minelli, Charles Oxnard, Chris Klingenberg, Mike Collyer, Philipp Mitteroecker, Carmelo Fruciano (again!), and Sarah Elton: with some of them, we are definitely on the same wavelength; with others, I fear we will have to agree that we may disagree!
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Cardini, A. Less tautology, more biology? A comment on “high-density” morphometrics. Zoomorphology 139, 513–529 (2020). https://doi.org/10.1007/s00435-020-00499-w
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DOI: https://doi.org/10.1007/s00435-020-00499-w