Research projects

Prof. Dr. Marcelo Sánchez
Comparative musculo-skeletal ontogeny of tetrapods
March 2007 to March 2018
Funding sources
SNF (Personen- und Projektförderung), Others
SNF 31003A-149605 (PI); previous funding: SNF 3100AO-116013/1 (PI); Leverhulme Foundation, UK (co-PI; PI: Dr. R. Asher, Cambridge)
Dr. Robert Asher (Cambridge University) (United Kingdom)
Dr. Ingmar Werneburg (Universität Tübingen) (Germany)
world map
The importance of evolutionary developmental biology (evo-devo) in bringing embryology to the evolutionary synthesis cannot be underestimated. However, the field is largely dominated by experimental approaches using model species and by molecular biology. More organismic and comparative approaches to study ontogeny are also experiencing a revival, addressing the old question of the impact of developmental studies in systematics. This kind of work is also benefiting from advances in experimental techniques and the incorporation of palaeontological data, and is in part inspired by the growing realization that the study of complex structures in time is fundamental to generate solid phylogenetic hypotheses based on morphological characters. This project aims at addressing this issue by studying heterochronies (changes in developmental timing) in the late development of selected Recent and fossil amniotes.

Examination of skeletal heterochronies in tetrapods are restricted to few taxa and have sampled either the skull or the postcranium. Already patterns were discovered, but they require testing with a wider sampling. The phylogenetic breadth examined in this project and the new methods employed would address questions such as: How conserved are ossification sequences among amniotes? Are heterochronic shifts connected to functional/ecological traits? How are these shifts related to morphological diversification?

The specific aims of this project can summarized as follows: (1) clear and stain and/or CT scan ontogenetic series obtained from Museum collections and experimental labs, including most major clades of mammals and turtles and representatives of most other major tetrapod clades; (2) produce the first comprehensive analysis of changes in developmental timing of the mammalian skeleton in a phylogenetic framework, as well as several other selected tetrapod clades; (3) test the utility of developmental timing data in reconstructing evolutionary relationships; (4) Describe the growth patterns in selected reptilian taxa from the fossil site of Monte San Giorgio.
Ontogeny, phylogeny, heterochrony, skeleton, muscle
Werneburg I, Sánchez-Villagra MR. 2015. Skeletal heterochrony is associated with the anatomical specializations of snakes among squamate reptiles. Evolution 69(1):254–263.
Werneburg I, Wilson LAB, Parr WCH, Joyce WG. 2015. Evolution of neck vertebral shape and neck retraction at the transition to modern turtles: an integrated geometric morphometric approach. Systematic Biology 64:187-204.
Fuchs M, Geiger M, Stange M, Sánchez-Villagra MR. 2015. Growth trajectories in the cave bear and its extant relatives: an examination of ontogenetic patterns in phylogeny. BMC Evolutionary Biology 15:239
Kolb C, Scheyer TM, Veitschegger K, Forasiepi AM, Amson E, van der Geer AAE, van den Hoek Ostende LW, Hayashi S, Sánchez-Villagra MR (2015) Mammalian bone palaeohistology: a survey and new data with emphasis on island forms. PeerJ 3:e1358
Kolb C, Scheyer TM, Lister AM, Azorit C, de Vos J, Schlingemann MAJ, Rössner GE, Monaghan NT, Sánchez-Villagra MR (2015) Growth in fossil and extant deer and implications for body size and life history evolution. BMC Evolutionary Biology 15:19
Amson E, Kolb C, Scheyer TM, Sánchez-Villagra MR (2015) Growth and life history of Middle Miocene deer (Mammalia, Cervidae) based on bone histology. Comptes Rendus Palevol 14:637-645.
Veitschegger K, Sánchez-Villagra MR. Tooth eruption sequences in cervids and the effect of morphology, life history and phylogeny. Journal of Mammalian Evolution. (in press)
Koyabu D, Werneburg I, Morimoto N, Zollikofer CPE, Forasiepi AM, Endo H, Kimura J, Ohdachi SD, Truong SN, Sánchez-Villagra MR. 2014. Mammalian skull heterochrony reveals modular evolution and a link between cranial development and brain size. Nat. Commun. 5:3625 [doi: 10.1038/ncomms4625].
Geiger M, Forasiepi AM, Koyabu D, Sánchez-Villagra MR. 2014. Heterochrony and postnatal growth in mammals – an examination of growth plates in limbs. Jour Evol Biol. 27:98–115.
Rager L, Hautier L, Forasiepi A, Goswami A, Sánchez-Villagra MR. 2014. Timing in cranial suture closure in placentals mammals: phylogenetic patterns, intraspecific variation and comparison with marsupials. Journal of Morphology. 275:125–140.
Werneburg I, Tzika AC, Hautier L, Asher RJ, Milinkovitch MC, Sánchez-Villagra MR. 2013. Development and embryonic staging in non-model organisms: the case of an afrotherian mammal. Journal of Anatomy 222:2-18.
Koyabu DB, Maier W, Sánchez-Villagra MR. 2012. Paleontological and developmental evidence resolve the homology and dual embryonic origin of a mammalian skull bone, the interparietal. PNAS 109:14075–14080.
Bickelmann C, Mitgutsch C, Richardson MK, Jiménez R, de Bakker MAG, Sánchez-Villagra MR. 2012. Transcriptional heterochrony in talpid mole autopods. Evo-Devo (BMC).
Hoyos JM, Carlini AC, Sánchez-Villagra MR, Mitgutsch CM. 2012. Skeletal development and adult osteology of Hypsiboas pulchellus (Anura: Hylidae). Acta Herpetologica 7:119-138.
Goswami A, Polly PD, Mock O, Sánchez-Villagra MR. 2012. Shape, variance and integration during craniogenesis: contrasting marsupial and placental mammals. Journal of Evolutionary Biology. 25:862-872.
Mitgutsch C, Richardson MK, Jiménez R, Martín JE, Kondrashov P, de Bakker MAG, Sánchez-Villagra MR. 2012. Circumventing the pentadactyly ‘constraint’ - autopodial recruitment of pre-axial structures in true moles. Biology Letters 8: 74-77.
Bärmann EV, Sánchez-Villagra MR. 2012. A phylogenetic study of late growth events in a mammalian evolutionary radiation - The cranial sutures of terrestrial cetartiodactyl mammals. Journal of Mammalian Evolution 19:43-56.
Hugi J, Scheyer TM. 2012. Ossification sequences and associated ontogenetic changes in the bone histology of pachypleurosaurids from Monte San Giorgio (Switzerland/Italy). Journal of Vertebrate Paleontology 32:315-327..
Hugi J, Sánchez-Villagra MR. 2012. Histological and skeletochronological analyses on life history and skeletal adaptations in the marine iguana Amblyrhynchus cristatus and in other iguanas. Journal of Herpetology 46:312-324.
Hugi J, Koyabu D, Hutchison MN, Sánchez-Villagra MR. 2012. Heterochronic shifts in the ossification sequences of surface and subsurface-dwelling skinks are correlated with the degree of limb reduction. Zoology 115:188-98.
Koyabu D, Endo H, Mitgutsch C, Suwa G, Catania KC, Zollikofer CPE, Oda S, Koyasu K, Ando M, Sánchez-Villagra MR. 2011. Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals. Evo Devo (BMC) 2011:221.
Werneburg I. 2011. The cranial musculature of turtles. Palaeontologia Electronica 14(2), 15A:99pp. [].
Wilson LAB, Sánchez-Villagra MR. 2011. The evolution and phylogenetic signal of growth trajectories: the case of chelid turtles. Journal of Experimental Zoology, Molecular and Developmental Evolution. 316:50–60.
Mitgutsch C, Wimmer C, Sánchez-Villagra MR, Hahnloser R, Schneider RA. 2011. Timing of ossification in duck, quail, and zebra finch: intraspecific variation, heterochronies, and life history evolution. Zoological Science 28: 491-500.
Werneburg I, Sánchez-Villagra MR. 2011. The Early Development of the Echidna, Tachyglossus aculeatus (Mammalia: Monotremata), and patterns of mammalian development. Acta Zoologica. 92: 75-88.
Hugi J, Scheyer TMS, Klein N, Sander M, Sánchez-Villagra MR. 2011. Long bone microstructure and life history data of pachypleurosaurids from the Middle Triassic of Monte San Giorgio, Switzerland/Italy. C R Paleovol. 10:413–426.
Sánchez-Villagra MR. 2010. Developmental palaeontology in synapsids: the rock record of ontogeny in mammals and their closest relatives. Proc. Roy. Soc. B. 277:1139-1147.
Sánchez-Villagra MR. 2010. Suture Closure as a Paradigm to Study Late Growth in Recent and Fossils Mammals: A Case Study with Giant Deer and Dwarf Deer Skulls. Journal of Vertebrate Paleontology 30:1895-1898.
Hautier L, Weisbecker V, Sánchez-Villagra MR, Goswami A, Asher RJ. 2010. Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proc Nat Acad Sci USA. 107:18903-18908.
Müller J, Scheyer TM, Head JJ, Barrett P, Werneburg I, Ericson PGP, Pol D, Sánchez-Villagra MR. 2010. Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes. Proc Nat Acad Sci USA. 107: 2118-2123.
Wilson LAB, Sánchez-Villagra MR. 2010. Diversity trends and their ontogenetic basis: an exploration of allometric disparity in rodents. Proc. Roy. Soc. B. 277:1227-1234.
Wilson LAB, Schradin C, Mitgutsch C, Galliari FC, Mess A, Sánchez-Villagra MR. 2010. Skeletogenesis in the African Striped Mouse (Rhabdomys pumilio) and a study of sequence heterochrony in rodent evolution. Organisms, Diversity and Evolution. 10:243-258.
Delfino M, Sánchez-Villagra MR. 2010. A survey of the rock record of reptilian ontogeny. In: Developmental Vertebrate Palaeontology (ed Sánchez-Villagra MR). Seminars in Cell and Developmental Biology 21:432-440.
Delfino M, Scheyer TM, Fritz U, Sánchez-Villagra MR. 2010. An integrative approach to examining a homology question: shell structures in soft-shell turtles. Biological Journal of the Linnean Society. 99:462-476.
Delfino M, Fritz U, Sánchez-Villagra MR. 2010. Evolutionary and developmental aspects of phalangeal formula variation in pig-nose and soft-shelled turtles (Carettochelyidae and Trionychidae). Organisms, Diversity and Evolution. 10:69-79.
Hugi J, Mitgutsch C, Sánchez-Villagra MR. 2010. Chondrogenic and ossification patterns in White's skink Liopholis whitii (Scincidae, Reptilia). Zoosystematics and Evolution. 86:21-32.
Galliari FC, Carlini AC, Sánchez-Villagra MR. 2010. Evolution of the axial skeleton in armadillos (Mammalia, Dasypodidae). Mammalian Biology. 75:326-333.
Richardson MK, Gobes S, Leeuwen A van, Poelman A, Pieau C, Sánchez-Villagra MR. 2009. Heterochrony in Limb Evolution: Developmental Mechanisms and Natural Selection. Journal of Experimental Zoology, Molecular and Developmental Evolution. 312B: 639-664. DOI: 10.1002/jez.b.21250.
Werneburg I, Sánchez-Villagra MR. 2009. Time of organogenesis support basal sauropsid position of turtles in the amniote tree of life. BMC Evolutionary Biology. 9:82 doi:10.1186/1471-2148-9-82.
Goswami A, V. Weisbecker V, Sánchez-Villagra MR. 2009. Developmental modularity and the marsupial-placental dichotomy. Journal of Experimental Zoology, Molecular and Developmental Evolution. 312B: 186-195.
Sánchez-Villagra MR, Müller H, Sheil CA, Scheyer TM, Nagashima H, Kuratani S. 2009. Skeletal Development in the Chinese soft-shelled turtle Pelodiscus sinensis (Reptilia: Testudines: Trionychidae). Journal of Morphology 270:1381–1399. DOI: 10.1002/jmor.10766.
Werneburg I, Hugi J, Müller J, Sánchez-Villagra MR. 2009. Embryogenesis and ossification of Emydura subglobosa (Testudines, Pleurodira, Chelidae) and patterns of turtle development. Developmental Dynamics. 238:2770-2786.
Wilson AB, Sánchez-Villagra MR. 2009. Heterochrony and Patterns of Cranial Suture Closure in Hystricognath Rodents. Journal of Anatomy 214:339-354.
Sánchez-Villagra MR, Anjali Goswami G, Weisbecker V, Mock O, Kuratani S. 2008. Conserved relative timing of cranial ossification patterns in early mammalian evolution. Evolution and Development. 10:519-530.
Asher RJ, Geisler JH, Sánchez-Villagra MR. 2008. Morphology, palaeontology, and placental mammal phylogeny. Systematic Biology. 57:311-317.
Weisbecker V, Goswami A, Wroe S, Sánchez-Villagra MR. 2008. Ossification heterochrony in the mammalian postcranial skeleton and the marsupial-placental dichotomy. Evolution. 62:2027-2041.
Scheyer TM, Brüllmann B, Sánchez-Villagra MR. 2008. The ontogeny of the shell in side-necked turtles, with emphasis on the homologies of costal and neural bones. Journal of Morphology 269:1008–1021.
Sánchez-Villagra MR, Ziermann JM, Olsson L. 2008. Limb chondrogenesis in Graptemys nigrinoda (Emydidae), with comments on the primary axis and the digital arch in turtles. Amphibia-Reptilia. 29:85-92.
Bininda-Emonds ORP, Jeffery JE, Sánchez-Villagra MR, Hanken J, Colbert M, Pieau C, Selwood L, Cate C t, Raynaud A, Osabutey CK, Richardson MK. 2007. Forelimb-hind limb developmental timing across tetrapods. BMC Evol. Biol. 7:182 (DOI:10.1186/1471-2148-7-182).
Sánchez-Villagra MR, Maier W. 2006. Homologies of the mammalian shoulder girdle – a response to Matsuoka et al. Evolution and Development 8:113-115.
Giannini N, Goswami A, Sánchez-Villagra MR. 2006. Development of integumentary structures in Rousettus amplexicaudatus (Mammalia: Chiroptera: Pteropodidae) during late-embryonic and fetal stages. Journal of Mammalogy 87(5), 993–1001.
Sánchez-Villagra MR, Maier W. 2003. Ontogenesis of the scapula in marsupial mammals, with special emphasis on perinatal stages of didelphids and remarks on the origin of the therian scapula. Journal of Morphology 258: 115-129.
Sánchez-Villagra MR. 2002. Comparative patterns of postcranial ontogeny in therian mammals: an analysis of relative timing of ossification events. Journal of Experimental Zoology: Molecular and Developmental Evolution 294:264-273.