Morphospace analysis leads to an evo-devo model of digit patterning.

Publisher: Wiley-Liss Country of Publication: United States NLM ID: 101168228 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1552-5015 (Electronic) Linking ISSN: 15525007 NLM ISO Abbreviation: J Exp Zool B Mol Dev Evol Subsets: MEDLINE

Original Publication: Hoboken, NJ : Wiley-Liss, c2003-

Biological Evolution*; Body Patterning/*physiology ; Forelimb/*anatomy & histology ; Lizards/*anatomy & histology ; Toes/*growth & development; Animals ; Body Patterning/genetics ; Forelimb/physiology ; Lizards/genetics ; Lizards/growth & development ; Models, Biological

Biological forms occupy a constrained portion of theoretical morphospaces. Developmental models accounting for empirical morphospaces are necessary to achieve a better understanding of this phenomenon. We analyzed the phalangeal formulas (PFs) in lizards and relatives' hands by comparing them with a set of simulated PFs that compose a theoretical morphospace. We detected that: (1) the empirical morphospace is severely limited in size, (2) the PFs comply with two properties of phalangeal count per digit, namely the ordering rule (DI ≤ DII ≤ DIII ≤ DIV ≥ DV), and the contiguity relationship (neighbor digits differ on average in one phalanx), (3) the totality of the PFs can be categorized into four categories of hands aligned along a feasibility gradient. We also reconstructed the evolution of PFs and found a stepwise trajectory from the plesiomorphic PF towards reduced conditions. Finally, we propose a developmental model as the generative mechanism behind the PFs. It is consistent with the bulk of evidence managed and involves an ordered digit primordia initialization timed with periodic signals of joint formation coming from digit tips. Our approach is also useful to address the study of other meristic sequences in nature such as dental, floral, and branchial formulas.
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Alberch, P. (1982). Developmental constraints in evolutionary processes. In J. T. Bonner (Ed.), Evolution and development. Springer-Verlag.
Avena-Koenigsberger, A., Goñi, J., Solé, R., & Sporns, O. (2015). Network morphospace. Journal of the Royal Society Interface, 12(103), 20140881. https://doi.org/10.1098/rsif.2014.0881.
Burke, A., & Feduccia, A. (1997). Developmental patterns and the identification of homologies in the avian hand. Science, 278, 666-668.
Caldwell, M. W. (2002). From fins to limbs to fins: Limb evolution in fossil marine reptiles. American Journal of Medical Genetics, 112(3), 236-249.
Coates, M. I. (1996). The Devonian tetrapod Acanthostega gunnari Jarvik: Postcranial anatomy, basal tetrapod interrelationships and patterns of skeletal evolution. Earth and Environmental Science Transactions of The Royal Society of Edinburgh, 87, 363-421.
Coates, M. I., & Ruta, M. (2007). Skeletal changes in the transition from fins to limbs. In B. K. Hall (Ed.), Fins into limbs: Evolution, development, and transformation (pp. 15-38). University of Chicago Press.
Cooper, K. L. (2015). Self-organization in the limb: A Turing mechanism for digit development. Current Opinion in Genetics and Development, 32, 92-97. https://doi.org/10.1016/j.gde.2015.02.001.
Cooper, L. N., Berta, A., Dawson, S. D., & Reidenberg, J. S. (2007). Evolution of hyperphalangy and digit reduction in the cetacean manus. The Anatomical Record, 290(6), 654-672.
Cooper, L. N., & Dawson, S. D. (2009). The trouble with flippers: A report on the prevalence of digital anomalies in Cetacea. Zoological Journal of the Linnean Society, 155, 722-735. https://doi.org/10.1111/j.1096-3642.2008.00454.x.
Dahn, R. D., & Fallon, J. F. (2000). Interdigital regulation of digit identity and homeotic transformation by modulated BMP signalling. Science, 289, 438-441.
Fedak, T. J., & Hall, B. (2004). Perspectives on hyperphalangy: Patterns and processes. Journal of Anatomy, 204, 151-163.
Fröbisch, N. B. (2008). Ossification patterns in the tetrapod limb: Conservation and divergence from morphogenetic events. Biological Reviews, 83(4), 571-600.
Galis, F., van Alphen, J. M., & Metz, J. A. J. (2001). Why five fingers? Evolutionary constraints on digit numbers. Trends in Ecology & Evolution, 16, 637-646. https://doi.org/10.1016/s0169-5347(01)/02289-3.
Gatesy, S. M., & Middleton, K. M. (2007). Skeletal adaptations for flight. In B. K. Hall (Ed.), Fins into limbs: Evolution, Development, and Transformation (pp. 284-309). University of Chicago Press.
Greer, A. E. (1991). Limb reduction in squamates: Identification of the lineages and discussion of the trends. Journal of Herpetology, 25, 166-173.
Greer, A. E. (1992). Hyperphalangy in squamates: Insight on the reacquisition of primitive character states in limb-reduced lineages. Journal of Herpetology, 26, 327-332.
Greer, A. E., & Cogger, H. (1985). Systematics of the reduce-limbed and limbless skinks currently assigned to the genus Anomalopus (Lacertilia: Scincidae). Records of the Australian Museum, 37(1), 11-54.
Greer, A. E., & Smith, S. (1999). Aspects of the morphology and reproductive biology of the Australian earless dragon lizard Tympanocryptis tetraporophora. Australian Journal of Zoology, 31, 55-70.
Hall, B. (2015). Bones and cartilage: Developmental and evolutionary skeletal biology, Chapter 40-Before limbs there were fins (2nd ed.). Academic Press.
Hiscock, T. W., Tschopp, P., & Tabin, C. J. (2017). On the formation of digits and joints during limb development. Developmental Cell, 41, 459-465. https://doi.org/10.1016/j.devcel.2017.04.021.
Huang, B. L., Trofka, A., Furusawa, A., Norrie, J. L., Rabinowitz, A. H., Vokes, S. A., Taketo, M. M., Zakany, J., & Mackem, S. (2016). An interdigit signalling centre instructs coordinate phalanx-joint formation governed by 5′ Hoxd-Gli3 antagonism. Nature Communications, 7, 12903. https://doi.org/10.1038/ncomms12903.
Kavanagh, K. D., Bailey, C. S., & Sears, K. E. (2020). Evidence of five digits in embryonic horses and developmental stabilization of tetrapod digit number. Proceedings of the Royal Society B: Biological Sciences. https://doi.org/10.1098/rspb.2019.2756.
Kavanagh, K. D., Shoval, O., Winslow, B. B., Alon, U., Leary, B. P., Kan, A., & Tabin, C. J. (2013). Developmental bias in the evolution of phalanges. Proceedings of the National Academy of Sciences of the United States of America, 110, 18190-18195. https://doi.org/10.1073/pnas.1315213110.
Kjaer, K. W., Hansen, L., Schwabe, G. C., Marques-de-Faria, A. P., Eiberg, H., Mundlos, S., Tommerup, N., & Rosenberg, T. (2005). Distinct CDH3 mutations cause ectodermal dysplasia, ectrodactyly, macular dystrophy (EEM syndrome). Journal of Medical Genetics, 42, 292-298.
Kohlsdorf, T., & Wagner, G. P. (2006). Evidence for the reversibility of digit loss: a phylogenetic study of limb evolution in Bachia (Gymnophthalmidae: Squamata). Evolution, 60(9), 1896-1912.
McGhee, G. R., Jr. (2007). The geometry of evolution, Adaptive landscapes and theoretical morphospaces. Cambridge University Press.
McGhee, G. R., Jr. (2015). Limits in the evolution of biological form: A theoretical morphologic perspective, Interface focus (Vol. 5, p. 20150034. https://doi.org/10.1098/rsfs.2015.0034.
Mehring, C., Akselrod, M., Bashford, L., Mace, M., Choi, H., Blüher, M., Buschhoff, A.-S., Pistohl, T., Salomon, R., Cheah, A., Blanke, O., Serino, A., & Burdet, E. (2019). Augmented manipulation ability in humans with six-fingered hands. Nature Communications, 10(1), 1-10. https://doi.org/10.1038/s41467-019-10306-w.
Mitteroecker, P., & Huttegger, S. M. (2009). The concept of morphospaces in evolutionary and developmental biology: Mathematics and metaphors. Biological Theory, 4, 54-67. https://doi.org/10.1162/biot.2009.4.1.54.
Morse, E. (1872). On the carpus and tarsus of birds. Annals of the Lyceum of Natural History of New-York, 10, 2-22.
Pascoal, S., Carvalho, C. R., Rodriguez-León, J., Delfini, M., Duprez, D., Thorsteinsdóttir, S., & Palmeirim, S. (2007). A molecular clock operates during chick autopod proximal-distal outgrowth. Journal of Molecular Biology, 368, 303-309. https://doi.org/10.1016/j.jmb.2007.01.089.
Pyron, R. A., Burbrink, F. T., & Wiens, J. J. (2013). A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13, 93-140.
R Core Team Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
Raskin-Gutman, D., & Izpisúa-Belmonte, J. C. (2004). Theoretical morphology of developmental asymmetries. BioEssays, 26, 405-412. https://doi.org/10.1002/bies.10410.
Raspopovic, J., Marcon, L., Russo, L., & Sharpe, J. (2014). Digit patterning is controlled by a Bmp-Sox9-Wnt Turing network modulated by morphogen gradients. Science, 345, 566-570. https://doi.org/10.1126/science.1252960.
Raup, D. M. (1966). Geometric analysis of shell coiling: General problems. Journal of Paleontology, 40, 1178-1190.
Ribeiro Sanches, P., dos Santos, F. P., & Costa-Campos, C. E. (2007). Ectrodactyly of the exotic lizard Hemidactylus mabouia (Squamata. Gekkonidae) in an urban area in Northern Brazil, Eastern Amazon. Boletín de la Asociación Herpetológica Española, 28, 13-14.
Richardson, M., & Chipman, A. (2003). Developmental constraints in a comparative framework: A test case using variations in phalanx number during amniote evolution. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 296, 8-22. https://doi.org/10.1002/jez.b.13.
Romer, A. S. (1956). Osteology of the reptiles. University of Chicago Press.
Salinas-Saavedra, M., Gonzalez-Cabrera, C., Ossa-Fuentes, L., Botelho, J. F., Ruiz-Flores, M., & Vargas, A. O. (2014). New developmental evidence supports a homeotic frameshift of digit identity in the evolution of the bird wing. Frontiers in Zoology, 11(1), 33.
Scoones, J. C., & Hiscock, T. W. (2020). A dot-stripe Turing model of joint patterning in the tetrapod limb. The Company of Biologists Ltd, 147, dev183699. https://doi.org/10.1242/dev.183699.
Shapiro, M., Shubin, N. H., & Downs, J. P. (2007). Limb reduction and diversity in reptilian evolution, Fins into limbs: Evolution, development and transformation. University of Chicago Press.
Shubin, N. H., & Alberch, P. (1986). A morphogenetic approach to the origin and basic organization of the tetrapod limb. Journal of Evolutionary Biology, 20, 3-387.
Shubin, N. H., & Fröbish, N. B. (2011). Salamander limb development: integrating genes, morphology, and fossils. Developmental Dynamics, 240, 1087-1099.
Suzuki, T., Hasso, S. M., & Fallon, J. F. (2014). Unique SMAD1/5/8 activity at the phalanx-forming region determines digit identity. Proceedings of the National Academy of Sciences of the United States of America, 150, 4185-4190. https://doi.org/10.1073/pnas.0707899105.
Tabin, C. J. (1992). Why we have (only) five fingers per hand: HOX genes and the evolution of paired limbs. Development, 116, 289-296.
Thewissen, M., & Taylor, J. (2007). Aquatic adaptations in the limb of Amniotes. In B. K. Hall (Ed.), Fins into limbs: Evolution, development, and transformation (pp. 310-322). University of Chicago Press.
Turing, A. M. (1952). The chemical basis of morphogenesis. Philosophical Transactions of the Royal Society, B: Biological Sciences, 237, 37-72.
Wagner, G. P., & Gauthier, J. A. (1999). 1,2,3=2,3,4: A solution to the problem of the homology of the digits in the avian hand. Proceedings of the National Academy of Sciences of the United States of America, 96(9), 511-5116.
Wagner, G. P., Griffith, O. W., Bergmann, P. J., Bello-Hellegouarch, G., Kohlsdorf, T., Buhllar, A., & Siler, C. D. (2018). Are there general laws for digit evolution in squamates? The loss and re-evolution of digits in a clade of fossorial lizards (Brachymeles, Scincinae). Journal of Morphology, 279(8), 1104-1119.
Young, R. L., Caputo, V., Giovannotti, M., Kohlsdorf, T., Vargas, A. O., May, G. E., & Wagner, G. P. (2009). Evolution of digit identity in the three-toed Italian skink Chalcides chalcides: A new case of digit identity frame shift. Evolution & Development, 11(6), 647-658.
Zhu, J., Nakamura, E., Nguyen, M. T., Bao, X., Akiyama, H., & Mackem, S. (2008). Uncoupling sonic hedgehog control of pattern and expansion of the developing limb bud. Developmental Cell, 14, 624-632. https://doi.org/10.1016/j.devcel.2008.01.008.

Keywords: constraints; digit patterning; empirical morphospace; network theory; phalangeal formula; theoretical morphospace

Date Created: 20210121 Date Completed: 20211014 Latest Revision: 20211014

20231215

10.1002/jez.b.23026

33476480