Abstract
Limb muscles are remarkably complex and evolutionarily labile. Although their anatomy is of great interest for studies of the evolution of form and function, their homologies among major amniote clades have remained obscure. Studies of adult musculature are inconclusive owing to the highly derived morphology of modern amniote limbs but correspondences become increasingly evident earlier in ontogeny. We followed the embryonic development of forelimb musculature in representatives of six major amniote clades and found, contrary to current consensus, that these early splitting patterns are highly conserved across Amniota. Muscle mass cleavage patterns and topology are highly conserved in reptiles including birds, irrespective of their skeletal modifications: the avian flight apparatus results from slight early topological modifications that are exaggerated during ontogeny. Therian mammals, while conservative in their cleavage patterns, depart drastically from the ancestral amniote musculoskeletal organization in terms of topology. These topological changes occur through extension, translocation and displacement of muscle groups later in development. Overall, the simplicity underlying the apparent complexity of forelimb muscle development allows us to resolve conflicting hypotheses about homology and to trace the history of each individual forelimb muscle throughout the amniote radiations.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
Confocal files have been deposited in Dryad (https://doi.org/10.5061/dryad.r2280gbd8)75.
References
Howell, A. B. Morphogenesis of the shoulder architecture. Part IV. Reptilia. Q. Rev. Biol. 11, 183–208 (1936).
Howell, A. B. Phylogeny of the distal musculature of the pectoral appendage. J. Morphol. 60, 287–315 (1936).
Howell, A. B. Morphogenesis of the shoulder architecture: Aves. Auk 54, 364–375 (1937).
Howell, A. B. Morphogenesis of the shoulder architecture. Part VI. Therian Mammalia. Q. Rev. Biol. 12, 440–463 (1937).
Howell, A. B. Morphogenesis of the shoulder architecture. Part V. Monotremata. Q. Rev. Biol. 12, 191–205 (1937).
Haines, R. W. A revision of the extensor muscles of the forearm in tetrapods. J. Anat. 73, 211 (1939).
Haines, R. W. The flexor muscles of the forearm and hand in lizards and mammals. J. Anat. 84, 13 (1950).
Straus, W. L. Jr The homologies of the forearm flexors: urodeles, lizards, mammals. Am. J. Anat. 70, 281–316 (1942).
Diogo, R., Abdala, V., Aziz, M., Lonergan, N. & Wood, B. From fish to modern humans—comparative anatomy, homologies and evolution of the pectoral and forelimb musculature. J. Anat. 214, 694–716 (2009).
Diogo, R. & Abdala, V. Muscles of Vertebrates: Comparative Anatomy, Evolution, Homologies and Development (CRC Press, 2010).
Abdala, V. & Diogo, R. Comparative anatomy, homologies and evolution of the pectoral and forelimb musculature of tetrapods with special attention to extant limbed amphibians and reptiles. J. Anat. 217, 536–573 (2010).
Diogo, R., Bello‐Hellegouarch, G., Kohlsdorf, T., Esteve‐Altava, B. & Molnar, J. L. Comparative myology and evolution of marsupials and other vertebrates, with notes on complexity, Bauplan, and “scala naturae”. Anat. Rec. 299, 1224–1255 (2016).
Russell, A. & Bauer, A. M. in Biology of the Reptilia Vol. 20 (eds Gaunt, A. et al.) 5–423 (Society for the Study of Amphibians and Reptiles, 2008).
Romer, A. S. Vertebrate Body (W.B. Saunders, 1970).
Romer, A. S. The development of the thigh musculature of the chick twelve figures. J. Morphol. 43, 347–385 (1927).
Romer, A. S. The development of tetrapod limb musculature—the thigh of Lacerta. J. Morphol. 71, 251–298 (1942).
Romer, A. S. The development of tetrapod limb musculature—the shoulder region of Lacerta. J. Morphol. 74, 1–41 (1944).
Walker, W. F. The development of the shoulder region of the turtle, Chrysemys picta marginata, with special reference to the primary musculature. J. Morphol. 80, 195–249 (1947).
Cheng, C. C. The development of the shoulder region of the opossum, Didelphys virginiana, with special reference to the musculature. J. Morphol. 97, 415–471 (1955).
Sullivan, G. Anatomy and embryology of the wing musculature of the domestic fowl (Gallus). Aust. J. Zool. 10, 458–518 (1962).
Kardon, G. Muscle and tendon morphogenesis in the avian hind limb. Development 125, 4019–4032 (1998).
Valasek, P., Evans, D. J., Maina, F., Grim, M. & Patel, K. A dual fate of the hindlimb muscle mass: cloacal/perineal musculature develops from leg muscle cells. Development 132, 447–458 (2005).
Valasek, P. et al. Somitic origin of the medial border of the mammalian scapula and its homology to the avian scapula blade. J. Anat. 216, 482–488 (2010).
Valasek, P. et al. Cellular and molecular investigations into the development of the pectoral girdle. Dev. Biol. 357, 108–116 (2011).
Huang, A. H. et al. Repositioning forelimb superficialis muscles: tendon attachment and muscle activity enable active relocation of functional myofibers. Dev. Cell 26, 544–551 (2013).
Pu, Q., Huang, R. & Brand‐Saberi, B. Development of the shoulder girdle musculature. Dev. Dyn. 245, 342–350 (2016).
Diogo, R., Siomava, N. & Gitton, Y. Development of human limb muscles based on whole-mount immunostaining and the links between ontogeny and evolution. Development 146, dev180349 (2019).
Watson, S. S., Riordan, T. J., Pryce, B. A. & Schweitzer, R. Tendons and muscles of the mouse forelimb during embryonic development. Dev. Dyn. 238, 693–700 (2009).
Christ, B. & Brand-Saberi, B. Limb muscle development. Int. J. Dev. Biol. 46, 905–914 (2004).
Chevallier, A., Kieny, M. & Mauger, A. Limb–somite relationship: origin of the limb musculature. Development 41, 245–258 (1977).
Fürbringer, M. Untersuchungen zur Morphologie und Systematik der Vögel: Zugleich ein Beitrag zur Anatomie der Stütz-und Bewegungsorgane (Verlag von TJ. van Holkema, 1888).
Meers, M. B. Crocodylian forelimb musculature and its relevance to Archosauria. Anat. Rec. 274, 891–916 (2003).
Vogel, A., Rodriguez, C., Warnken, W. & Belmonte, J. C. I. Dorsal cell fate specified by chick Lmxl during vertebrate limb development. Nature 378, 716–720 (1995).
Schäfer, K. & Braun, T. Early specification of limb muscle precursor cells by the homeobox gene Lbx1h. Nat. Genet. 23, 213–216 (1999).
Kardong, K. V. Vertebrates: Comparative Anatomy, Function, Evolution (McGraw-Hill, 2006).
Ziermann, J. M. & Diogo, R. Cranial muscle development in frogs with different developmental modes: direct development versus biphasic development. J. Morphol. 275, 398–413 (2014).
Diogo, R. & Ziermann, J. M. Development of fore‐ and hindlimb muscles in frogs: morphogenesis, homeotic transformations, digit reduction, and the forelimb–hindlimb enigma. J. Exp. Zool. B 322, 86–105 (2014).
Nagashima, H. et al. Evolution of the turtle body plan by the folding and creation of new muscle connections. Science 325, 193–196 (2009).
Botelho, J. F., Smith-Paredes, D., Nuñez-Leon, D., Soto-Acuna, S. & Vargas, A. O. The developmental origin of zygodactyl feet and its possible loss in the evolution of Passeriformes. Proc. R. Soc. B 281, 20140765 (2014).
Walker, W. Jr in Biology of the Reptilia Vol. 4 (ed. Gans, C.) 1–100 (Academic Press, 1973).
Romer, A. S. The locomotor apparatus of certain primitive and mammal-like reptiles. Bull. Am. Mus. Nat. Hist. 46, 517–606 (1922).
Sewertzoff, A. Studien über die Entwickelung der Muskeln, Nerven und des Skeletts der Extremitäten der niederen Tetrapoda: Beiträge zu einer Theorie der pentadactylen Extremität der Wirbeltiere (Typo-lithogr. de la Société JN Kouchnéreff, 1908).
George, J. C. & Berger, A. J. (eds) Avian Myology (Academic Press, 1966).
Van den Berge, J. in Handbook of Avian Anatomy: Nomina Anatomica Avium 2nd edn (eds Baumel, J. J. et al.) 189–247 (Nuttall Ornithological Club, 1993).
Warburton, N. Functional Morphology and Evolution of Marsupial Moles (Marsupialia: Notoryctemorphia). PhD thesis, Univ. Western Australia (2003).
Jenkins, P. A. & Weijs, W. The functional anatomy of the shoulder in the Virginia opossum (Didelphis virginiana). J. Zool. 188, 379–410 (1979).
Botelho, J. F. et al. New developmental evidence clarifies the evolution of wrist bones in the dinosaur–bird transition. PLoS Biol. 12, e1001957 (2014).
Cihak, R. Ontogenesis of the Skeleton and Intrinsic Muscles of the Human Hand and Foot (Springer Science & Business Media, 2013).
Huang, A. H. et al. Musculoskeletal integration at the wrist underlies the modular development of limb tendons. Development 142, 2431–2441 (2015).
Holmes, R. The osteology and musculature of the pectoral limb of small captorhinids. J. Morphol. 152, 101–140 (1977).
McKay, W. J. S. The Morphology of the Muscles of the Shoulder-Girdle in Monotremes (Linnean Society of New South Wales, 1894).
Shrivastava, R. The deltoid musculature of the Monotremata. Am. Midl. Nat. 67, 434–440 (1962).
Regnault, S., Fahn-Lai, P., Norris, R. M. & Pierce, S. E. Shoulder muscle architecture in the Echidna (Monotremata: Tachyglossus aculeatus) indicates conserved functional properties. J. Mammal. Evol. 27, 591–603 (2020).
Diogo, R. & Tanaka, E. M. Development of fore‐and hindlimb muscles in GFP‐transgenic axolotls: morphogenesis, the tetrapod bauplan, and new insights on the forelimb–hindlimb enigma. J. Exp. Zool. B 322, 106–127 (2014).
Diogo, R., Walsh, S., Smith, C., Ziermann, J. M. & Abdala, V. Towards the resolution of a long‐standing evolutionary question: muscle identity and attachments are mainly related to topological position and not to primordium or homeotic identity of digits. J. Anat. 226, 523–529 (2015).
Matsuoka, T. et al. Neural crest origins of the neck and shoulder. Nature 436, 347–355 (2005).
Chevallier, A. & Kieny, M. On the role of the connective tissue in the patterning of the chick limb musculature. Rouxs Arch. Dev. Biol. 191, 277–280 (1982).
Mauger, A., Kieny, M., Hedayat, I. & Goetinck, P. F. Tissue interactions in the organization and maintenance of the muscle pattern in the chick limb. Development 76, 199–215 (1983).
Kardon, G., Harfe, B. D. & Tabin, C. J. A Tcf4-positive mesodermal population provides a prepattern for vertebrate limb muscle patterning. Dev. Cell 5, 937–944 (2003).
Tozer, S. et al. Involvement of vessels and PDGFB in muscle splitting during chick limb development. Development 134, 2579–2591 (2007).
Hurren, B., Collins, J. J., Duxson, M. J. & Deries, M. First neuromuscular contact correlates with onset of primary myogenesis in rat and mouse limb muscles. PLoS ONE 10, e0133811 (2015).
Deries, M. & Thorsteinsdóttir, S. Axial and limb muscle development: dialogue with the neighbourhood. Cell. Mol. Life Sci. 73, 4415–4431 (2016).
Kin, K., Maziarz, J. & Wagner, G. P. Immunohistological study of the endometrial stromal fibroblasts in the opossum, Monodelphis domestica: evidence for homology with eutherian stromal fibroblasts. Biol. Reprod. 90, 111–112 (2014).
Griffith, O. W. et al. Endometrial recognition of pregnancy occurs in the grey short-tailed opossum (Monodelphis domestica). Proc. R. Soc. B 286, 20190691 (2019).
McCrady, E. Embryology of the Opossum (Wistar Institute of Anatomy, 1938).
Ainsworth, S. J., Stanley, R. L. & Evans, D. J. Developmental stages of the Japanese quail. J. Anat. 216, 3–15 (2010).
Ferguson, M. W. The reproductive biology and embryology of the crocodilians. Biol. Reptilia 12, 330–491 (1981).
Noro, M., Uejima, A., Abe, G., Manabe, M. & Tamura, K. Normal developmental stages of the Madagascar ground gecko Paroedura pictus with special reference to limb morphogenesis. Dev. Dyn. 238, 100–109 (2009).
Smith‐Paredes, D., Lord, A., Meyer, D. & Bhullar, B. A. S. A developmental staging system and musculoskeletal development sequence of the Common Musk turtle (Sternotherus odoratus). Dev. Dyn. 250, 111–127 (2021).
Zheng, H. & Rinaman, L. Simplified CLARITY for visualizing immunofluorescence labeling in the developing rat brain. Brain Struct. Funct. 221, 2375–2383 (2016).
Renier, N. et al. iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159, 896–910 (2014).
Yang, B. et al. Single-cell phenotyping within transparent intact tissue through whole-body clearing. Cell 158, 945–958 (2014).
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676 (2012).
Theis, S. et al. The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature. Development 137, 2961–2971 (2010).
Smith Paredes, D. Embryonic muscle splitting patterns reveal homologies of amniote forelimb muscles. Dryad https://doi.org/10.5061/dryad.r2280gbd8 (2022).
Acknowledgements
We would like to thank R. Elsey for her help in collecting alligator eggs and M. Bradford for his help in obtaining musk turtle eggs. We also want to thank Yale’s Institute for Biospheric Studies (YIBS) and the Yale Peabody Museum of Natural History for funding this research.
Author information
Authors and Affiliations
Contributions
D.S.-P. conceived the study, cared for and maintained the colony of P. pictus, collected eggs and embryos of all reptile species, performed immunostaining experiments and imaged the samples, processed the files and segmented them in VGStudio, created the figures and wrote the manuscript. M.E.V.-C. cared for and maintained the colony of P. pictus, collected eggs and embryos of P. pictus, bred and collected embryos of M. domestica, performed immunostaining experiments, imaged, processed and segmented in VGStudio all M. domestica samples. A.L. collected S. odoratus embryos. M.M.M. and R.R.B. bred and collected embryos of M. musculus. B.-A.S.B. provided logistical and financial support for the reptile colony, embryo collection, immunostaining, microscopic imaging and digital segmentation of the samples and helped write the manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature Ecology & Evolution thanks Hiroshi Nagashima, Virginia Abdala and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data
Extended Data Fig. 1 Homologies of the dorsal musculature of the forelimb in Amniota.
Homologies of the dorsal musculature of the forelimb in Amniota. Muscles in individual rows are inferred to be homologous across clades based on their embryological origin and cleavage pattern from the divisions and subdivisions identified in the species studied. Rows containing more than one muscle per taxa reference cases in which the distinction of the muscles are not clear or individual portions of one muscle can be homologized to individual muscles of another group. Each muscle is named according to the nomenclature proposed by the authors listed under the clade names. Names proposed for reptilian musculature by Abdala and Diogo, 2010, are listed below if the nomenclature is not the same as in the other studies or they refer to a muscle complex.
Extended Data Fig. 2 Homologies of the ventral musculature of the forelimb in Amniota.
Homologies of the ventral musculature of the forelimb in Amniota. Muscles in individual rows are inferred to be homologous across clades based on their embryological origin and cleavage pattern from the divisions and subdivisions identified in the species studied. Rows containing more than one muscle per taxa reference cases in which the distinction of the muscles are not clear or individual portions of one muscle can be homologized to individual muscles of another group. Each muscle is named according to the nomenclature proposed by the authors listed under the clade names. Names proposed for reptilian musculature by Abdala and Diogo, 2010, are listed below if the nomenclature is not the same as in the other studies or they refer to a muscle complex.
Extended Data Fig. 3 Development of the forelimb musculature of reptiles, with focus on the ventral extrinsic musculature.
Development of the forelimb musculature of reptiles, with focus on the ventral extrinsic musculature derived from the Pectoralis (dark green) and Supracoracoideus (light green) divisions. All views ventral, except Paroedura PO 22 that is lateral and Coturnix HH33-34 that is a medial view. The Supracoracoideus division usually lays anterior to the Pectoralis division; in Coturnix in turn, it has shifted deep to it and extends into the humerus forming a pronounced curve. The proximal portion forms M. supracoracoideus (empty light green arrow) while the distal portion, beyond the curve, forms M. tensor propatagialis (light green arrow). PD: Pectoralis division, sc: M. supracoracoideus, SCD: Supracoracoid division, tpp: M. tensor propatagialis. All scale bars are 500 µm.
Extended Data Fig. 4 Development of the forelimb musculature of reptiles, with focus on the dorsal extrinsic musculature.
Development of the forelimb musculature of reptiles, with focus on the dorsal extrinsic musculature derived from the Latissimus (dark red), Deltoid (red) and Subscapular (magenta) divisions. All images show lateral view, except for the second row of Coturnix showing medial views of the forelimb musculature. The empty red arrows and the red arrows point at the development of the scapular and clavicular lobes of the Deltoid division respectively. In Sternotherus, like in some other turtles, the scapular portion does not form. The empty dark-red arrow points at the anterior lobe formed from the Latissimus division. In Alligator, this gives rise to the Teres major muscle (tm). In Chrisemys, as described by Walker 1947, this also gives rise to M. teres major. In Sternotherus, this muscle does not seem to develop, although in stage 16 an incipient anterior lobe of the Latissimus division, comparable to that of Alligator can be observed (tm?). In Coturnix, the Latissimus division divides (although slightly later) into two lobes, giving rise to the anterior (tm?) and posterior heads of the latissimus muscle. This sort of lobation is not observed in Paroedura and no comparable muscle develops in lizards. The empty magenta arrow points at M. subscapularis (M. scapulohumeralis caudalis of birds). dc: M. deltoideus clavicularis, DD: Deltoid division, ds: M. deltoideus scapularis, ld: M. latissimus dorsii, ldp: M. latissimus dorsii posterior, LD: Latissimus division, shc: M. scapulohumeralis caudalis, sbcc: M. subcoracoideus, sbsc: M. subscapularis, SSD: Subscapular division, tm: M. teres major, *: M. scapulohumeralis anterior. All scale bars are 500 µm.
Extended Data Fig. 5 Development of the forelimb musculature of therian mammals with focus on the ventral extrinsic musculature.
Development of the forelimb musculature of therian mammals, Mus and Monodelphis, with focus on the ventral extrinsic musculature derived from the Pectoral (dark green) and Supracoracoideus (light green) divisions. The Pectoralis division originates M. panniculus carnosus (white bordered dark green arrow), M. pectoralis minor (empty dark green arrow) and the deep portion of M. pectoralis major (dark green arrow). The ventral portion of the Supracoracoideus division forms the superficial portion of M. pectoralis major (empty light green arrow) and the clavicular deltoid (light green arrow). The dorsal extension of the Supracoracoideus division invades the dorsal aspect of the scapula (*) and bifurcates around the scapular spine (**) originating M. supraspinatus (yellow bordered light green arrow) and M. infraspinatus (red bordered light green arrow). The upper series of mouse embryos depicts a medial view of stage E12.0, a lateral view of stage E12.5 and ventral views of E13.5 and 14.5. Bottom series of Monodelphis and Mus show the developing embryos with all muscle groups except for those deriving from the Pectoral and Supracoracoideus divisions removed, and the developing skeleton stained with either Sox9 or Col II antibodies. M. panniculus carnosus was removed from Monodelphis MC 33 and 33+ and Mus E14.5. dc: M. deltoideus clavicularis, isp: M. infraspinatus, pc: M. panniculus carnosus, PD: Pectoralis division, pmi: M. pectoralis minor, pmp: M. pectoralis major profundus, pms: M. pectoralis major superficialis, ssp: M. supraspinatus. All scale bars are 500 µm.
Extended Data Fig. 6 Development of the forelimb musculature of therian mammals with focus on the dorsal extrinsic musculature.
Development of the forelimb musculature of therian mammals, Mus and Monodelhpis, with focus on the dorsal extrinsic musculature derived from the Latissimus (dark red), Deltoid (bright red) and Subscapular (magenta) divisions. As in reptiles, the Deltoid division of mice cleaves early into two lobes, forming M. scapulodeltoid (red arrow) and M. teres minor (empty red arrow). In Monodelphis a Teres minor muscle was not observed. The posterior portion of the Subscapular division extends along the posterior margin and lateral surface of the scapula (*), forming M. teres major (empty magenta arrow). The upper series shows Mus embryos between E12.0 and 14.5, all in lateral view. The bottom series of Monodelphis and Mus show the development of the muscles and skeleton in lateral view. M. latissimus dorsii is not shown in mice E14.5. DD: Deltoid division, ds: M. deltoideus scapularis, ld: M. latissimus dorsii, LD: Latissimus division, ssc: M. subscapularis, SSD: Subscapular division, tm: M. teres major, tmi: M. teres minor. All scale bars are 500 µm.
Extended Data Fig. 7 Development of the forelimb musculature of amniotes, with focus on the dorsal intrinsic musculature.
Development of the forelimb musculature of amniotes, with focus on the dorsal intrinsic musculature derived from the Triceps (light yellow) and Extensor (yellow) divisions. Note the distal extension of the Triceps division along the ulna, originating the posterior-most extensor muscle of the forearm (empty light-yellow arrow), and the humeral lobe of the Extensor division, extending proximally along the humerus (yellow arrow) and forming M. brachialis of lizards, turtles, birds and mammals, homologous to M. humeroradialis of crocodylians. Mm. dorsoepitrochlearis (light-yellow arrow) of mammals derives from the Triceps subdivision. c: central lobe (posterior-most lobe) of the Extensor division, dep: M. dorsoepitrochlearis, h: humeral lobe of the Extensor subdivision, r: radial lobe of the Extensor subdivision, u: “ulnar” lobe of the forearm musculature, derived from the Triceps subdivision. All scale bars are 500 µm.
Extended Data Fig. 8 Development of the forelimb musculature of amniotes, with focus on the brachial muscles that act as flexors of the forearm.
Development of the forelimb musculature of amniotes, with focus on the brachial muscles that act as flexors of the forearm. From the Extensor division, on the dorsal forearm, a muscle extends proximally over the humerus (yellow arrow) forming M. brachialis of Paroedura, Sternotherus, Coturnix and Mus, homologous to M. humeroradialis of Alligator. On the other hand, the biceps muscle and the crocodylians M. brachialis derive from the Brachial subdivision (empty blue arrow). bi: M. biceps brachii, br: M. brachialis (note that the muscle termed “brachialis” derive from different origins than in the other species in Alligator), hr: M. humeroradialis (note that the humeroradialis muscle derives from the same portion of the Brachial subdivision than the brachialis muscles of the other species). All scale bars are 500 µm.
Extended Data Fig. 9 Development of the forelimb musculature of amniotes, with focus on the intrinsic musculature deriving from the Flexor division.
Development of the forelimb musculature of amniotes, with focus on the intrinsic musculature deriving from the Flexor division (light blue). The Flexor division forms a deep lobe, and superficially a central lobe (empty light-blue arrow), flanked by an ulnar lobe on the ulnar side of the forearm (bottom portion of each arm in the images) and a radial lobe on the radial side (top). Note that the central lobe of the Flexor subdivision (pointed at by the empty light-blue arrow and originating M. flexor digitorum longus/communis) is the source of the so-called M. flexor carpi radialis of mice, otherwise originated from the radial lobe in other species. M. palmaris longus of Sternotherus, derives from the central lobe too, while its homonym derives from the ulnar lobe in mice. c: central lobe of the Flexor subdivision, d: deep lobe of the Flexor subdivision, epa: M. epitrochleoanconeus, fcra: M. flexor carpi radialis, fcu: M. flexor carpi ulnaris, fdc: M. flexor digitorum comunis, fdl: M. flexor digitorum longus, pal: M. palmaris longus, prop: M. pronator profundus, pros: M. pronator superficialis, prot: M. pronator teres, r: radial lobe of the Flexor subdivision, u: ulnar lobe of the Flexor subdivision. All scale bars are 500 µm.
Extended Data Fig. 10 Development of the forelimb musculature of amniotes, with focus on the ventral hand musculature deriving from the Hand flexor division.
Development of the forelimb musculature of amniotes, with focus on the ventral hand musculature deriving from the Hand flexor division (dark blue). The hand flexor musculature derives from the distal portion of the Flexor division and stratifies into layers; a superficial one (white bordered blue arrow) forms two layers of muscles, usually grouped as the Mm. flexores digitorum breves. M. lumbricales (*) of the mouse seem to develop from this portion of the Hand flexor division. A deeper layer (light-blue bordered dark blue arrow), also stratified, forms the deepest sets of muscles, termed lumbricales and interossei dorsales and ventrales. In the mouse, the most-superficial set of hand flexor muscles (coloured white in E15.5) elongates and translocates proximally into the forearm to form M. flexor digitorum superficialis. Deriving from the HF, a group of muscles extends dorsally in between the metacarpals in Monodelphis stages MC 33 + and 34 (red bordered blue arrows), likely precursors of M. flexor digitorum breves profundi and/or M. intermetacarpales. Note that the Hand extensor musculature fails to develop as observed in a dorsal view of the mouse forearm in E14.5 and of the short-tailed opossum MC stages 33+ and 34. Also, both the dorsal and ventral hand musculature is conspicuously reduced in Coturnix, developing from a non-stratified muscle division and forming considerable fewer muscles than in other reptiles. DL: deep layer of the Hand flexor subdivision, fbp: M. flexores digitroum breves profundi, fdl: humeral head of M. flexor digitorum longus, fdlu: ulnar head of M. flexor digitorum longus, fds: M. flexor digitorum superficialis, SL: superficial layer of Hand flexor subdivision, *: M. lumbricales. All scale bars are 500 µm.
Supplementary information
Rights and permissions
About this article
Cite this article
Smith-Paredes, D., Vergara-Cereghino, M.E., Lord, A. et al. Embryonic muscle splitting patterns reveal homologies of amniote forelimb muscles. Nat Ecol Evol 6, 604–613 (2022). https://doi.org/10.1038/s41559-022-01699-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41559-022-01699-x