Abstract
Mammals have an evolutionary history spanning hundreds of millions of years. Today, mammals represent one of the most diverse groups of tetrapod vertebrates. In particular, they present a great postural diversity. The humerus adopts different positions: small mammals have a “crouched” posture with a quasi-horizontal humerus, while in the largest species, the humerus is more vertical. Some monotremes have more transversely oriented humeri similar to those of reptiles. The forelimb of moles is also modified in relation to their burrowing lifestyle. This postural diversity is accompanied by an important microanatomical disparity. Indeed, the bones of the appendicular skeleton support the weight of the body and are subjected to various forces that partly shape their external and internal morphology. We show here how geometric and microanatomical parameters measured in cross-section such as the polar section modulus or the position of the medullo-cortical transition can be related to posture. Using statistical methods that take phylogeny into account, we develop a postural model from a sample of humerus cross-sections belonging to 41 species of extant mammals. Our model can be used by palaeontologists to infer the posture of extinct synapsids. As an example, we infer the posture of two emblematic taxa: Dimetrodon natalis and Peratherium cuvieri. The results of the analysis indicate a sprawling posture for Dimetrodon and a crouched posture for Peratherium. This work contributes to unravel the complex interaction between phylogeny, humeral microanatomy and geometry, body mass, lifestyle and posture in mammals.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data that support the findings of this study are included in this published article and its online resources.
Change history
18 April 2023
A Correction to this paper has been published: https://doi.org/10.1007/s10914-023-09659-3
References
Abbott CP (2019) The Dimetrodon dilemma: reassessing posture in sphenacodontians and related non-mammalian synapsids. Undergraduate honors dissertation, College of William and Mary
Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42
Alboukadel K (2021) rstatix: pipe-friendly framework for basic statistical tests. R package version 0.7.0
Amson E, Kolb C (2016) Scaling effect on the mid-diaphysis properties of long bones—the case of the Cervidae (deer). Sci Nat 103:1–10. https://doi.org/10.1007/s00114-016-1379-7
Amson E, de Muizon C, Laurin M, Argot C, de Buffrénil V (2014) Gradual adaptation of bone structure to aquatic lifestyle in extinct sloths from Peru. Proc R Soc Lond B Biol Sci 281:20140192. https://doi.org/10.1098/rspb.2014.0192
Argot C (2001) Functional-adaptive anatomy of the forelimb in the Didelphidae, and the paleobiology of the Paleocene marsupials Mayulestes ferox and Pucadelphys andinus. J Morphol 247:51–79. https://doi.org/10.1002/1097-4687(200101)247:1<51::AID-JMOR1003>3.0.CO;2-%23
Bakker RT (1971) Dinosaur physiology and the origin of mammals. Evolution 25:636–658. https://doi.org/10.1111/j.1558-5646.1971.tb01922.x
Beck TJ, Ruff CB, Mourtada FA, Shaffer RA, Maxwell-Williams K, Kao GL, Sartoris DJ, Brodine S (1996) Dual-energy X-ray absorptiometry derived structural geometry for stress fracture prediction in male U.S. marine corps recruits. J Bone Miner Res 11:645–653. https://doi.org/10.1002/jbmr.5650110512
Benton MJ (2015) Vertebrate Palaeontology. Wiley, Hoboken
Biewener AA (1989a) Mammalian terrestrial locomotion and size. Bioscience 39:776–783. https://doi.org/10.2307/1311183
Biewener AA (1989b) Scaling body support in mammals: limb posture and muscle mechanics. Science 245:45–48. https://doi.org/10.1126/science.2740914
Biewener AA (1990) Biomechanics of mammalian terrestrial locomotion. Science 250:1097–1103. https://doi.org/10.1126/science.2251499
Biewener AA (2005) Biomechanical consequences of scaling. J Exp Biol 208:1665–1676. https://doi.org/10.1242/jeb.01520
Bishop PJ, Hocknull SA, Clemente CJ, Hutchinson JR, Barrett RS, Lloyd DG (2018a) Cancellous bone and theropod dinosaur locomotion. Part II—a new approach to inferring posture and locomotor biomechanics in extinct tetrapod vertebrates. PeerJ 6:e5779. https://doi.org/10.7717/peerj.5779
Bishop PJ, Hocknull SA, Clemente CJ, Hutchinson JR, Farke AA, Barrett RS, Lloyd DG (2018b) Cancellous bone and theropod dinosaur locomotion. Part III—inferring posture and locomotor biomechanics in extinct theropods, and its evolution on the line to birds. PeerJ 6:e5777. https://doi.org/10.7717/peerj.5777
Bishop PJ, Hocknull SA, Clemente CJ, Hutchinson JR, Farke AA, Beck BR, Barrett RS, Lloyd DG (2018c) Cancellous bone and theropod dinosaur locomotion. Part I—an examination of cancellous bone architecture in the hindlimb bones of theropods. PeerJ 6:e5778. https://doi.org/10.7717/peerj.5778
Blob RW (2000) Interspecific scaling of the hindlimb skeleton in lizards, crocodilians, felids and canids: does limb bone shape correlate with limb posture? J Zool 250:507–531. https://doi.org/10.1111/j.1469-7998.2000.tb00793.x
Blob RW (2001) Evolution of hindlimb posture in nonmammalian therapsids: biomechanical tests of paleontological hypotheses. Paleobiology 27:14–38. https://doi.org/10.1666/0094-8373(2001)0272.0.CO;2
Blob RW, Biewener AA (1999) In vivo locomotor strain in the hindlimb bones of Alligator mississippiensis and Iguana iguana: implications for the evolution of limb bone safety factor and non-sprawling limb posture. J Exp Biol 202:1023–1046. https://doi.org/10.1242/jeb.202.9.1023
Blob RW, Biewener AA (2001) Mechanics of limb bone loading during terrestrial locomotion in the green iguana (Iguana iguana) and American alligator (Alligator mississippiensis). J Exp Biol 204:1099–1122. https://doi.org/10.1242/jeb.204.6.1099
Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745. https://doi.org/10.1111/j.0014-3820.2003.tb00285.x
Borges R, Machado JP, Gomes C, Rocha AP, Antunes A (2019) Measuring phylogenetic signal between categorical traits and phylogenies. Bioinformatics 35:1862–1869. https://doi.org/10.1093/bioinformatics/bty800
Brocklehurst N, Kammerer CF, Fröbisch J (2013) The early evolution of synapsids, and the influence of sampling on their fossil record. Paleobiology 39:470–490. https://doi.org/10.1666/12049
Brocklehurst RJ, Fahn-Lai P, Regnault S, Pierce SE (2022) Musculoskeletal modeling of sprawling and parasagittal forelimbs provides insight into synapsid postural transition. iScience 25:103578. https://doi.org/10.1016/j.isci.2021.103578
Butcher MT, Espinoza NR, Cirilo SR, Blob RW (2008) In vivo strains in the femur of river cooter turtles (Pseudemys concinna) during terrestrial locomotion: tests of force-platform models of loading mechanics. J Exp Biol 211:2397–2407. https://doi.org/10.1242/jeb.018986
Butcher MT, White BJ, Hudzik NB, Gosnell WC, Parrish JH, Blob RW (2011) In vivo strains in the femur of the Virginia opossum (Didelphis virginiana) during terrestrial locomotion: testing hypotheses of evolutionary shifts in mammalian bone loading and design. J Exp Biol 214:2631–2640. https://doi.org/10.1242/jeb.049544
Campione NE, Evans DC (2012) A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biol 10:1–22. https://doi.org/10.1186/1741-7007-10-60
Canoville A, Laurin M (2009) Microanatomical diversity of the humerus and lifestyle in lissamphibians. Acta Zool 90:110–122. https://doi.org/10.1111/j.1463-6395.2008.00328.x
Canoville A, Laurin M (2010) Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on palaeobiological inferences. Biol J Linn Soc Lond 100:384–406. https://doi.org/10.1111/j.1095-8312.2010.01431.x
Canoville A, de Buffrénil V, Laurin M (2021) Bone microanatomy and lifestyle in tetrapods. In: de Buffrénil V, de Ricqlès AJ, Zylberberg L, Padian K, Laurin M, Quilhac A (eds) Vertebrate Skeletal Histology and Paleohistology. CRC Press, Boca Raton, pp 724–743
Carrano MT (1999) What, if anything, is a cursor? Categories versus continua for determining locomotor habit in mammals and dinosaurs. J Zool 247:29–42. https://doi.org/10.1111/j.1469-7998.1999.tb00190.x
Cavanaugh T (2021) Reconstructing body size and center of mass in synapsids. Dissertation, Harvard University
Charig AJ (1972) The evolution of the archosaur pelvis and hindlimb: an explanation in functional terms. In: Joysey KA, Kemp TS (eds) Studies in Vertebrate Evolution. Oliver and Boyd, Edinburgh, pp 121–155
Cooper LN, Clementz MT, Usip S, Bajpai S, Hussain ST, Hieronymus TL (2016) Aquatic habits of cetacean ancestors: integrating bone microanatomy and stable isotopes. Integr Comp Biol 56:1370–1384. https://doi.org/10.1093/icb/icw119
Currey JD (2013) Bones: Structure and Mechanics. Princeton University Press, Princeton. https://doi.org/10.1515/9781400849505
D’Août K, Vereecke EE, Schoonaert K, De Clercq D, Van Elsacker L, Aerts P (2004) Locomotion in bonobos (Pan paniscus): differences and similarities between bipedal and quadrupedal terrestrial walking, and a comparison with other locomotor modes. J Anat 204:353–361. https://doi.org/10.1111/j.0021-8782.2004.00292.x
Debuysschere M (2015) Origine et première diversification des mammaliaformes : apport des faunes du Trias supérieur de Lorraine, France. Dissertation, Muséum national d’Histoire naturelle, Paris
Desmond AJ (1975) The Hot-Blooded Dinosaurs. Blond and Briggs, London
Didier G, Laurin M (2020) Exact distribution of divergence times from fossil ages and tree topologies. Syst Biol 69:1068–1087. https://doi.org/10.1093/sysbio/syaa021
Doube M, Klosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, Jackson JS, Schmid B, Hutchinson JR, Shefelbine SJ (2010) BoneJ: free and extensible bone image analysis in ImageJ. Bone 47:1076–1079. https://doi.org/10.1016/j.bone.2010.08.023
Everitt BS, Skrondal A (2010) The Cambridge Dictionary of Statistics. Cambridge University Press, Cambridge
Fabbri M, Navalón G, Benson RBJ, Pol D, O’Connor J, Bhullar BAS, Erickson GM, Norell MA, Orkney A, Lamanna MC, Zouhri S, Becker J, Emke A, Dal Sasso C, Bindellini G, Maganuco S, Auditore M, Ibrahim N (2022) Subaqueous foraging among carnivorous dinosaurs. Nature 603:1–6. https://doi.org/10.1038/s41586-022-04528-0
Gambaryan PP, Kielan-Jaworowska Z (1997) Sprawling versus parasagittal stance in multituberculate mammals. Acta Palaeontol Pol 42:13–44
Gambaryan PP, Kuznetsov AN (2013) An evolutionary perspective on the walking gait of the long-beaked echidna. J Zool 290:58–67. https://doi.org/10.1111/jzo.12014
Gatesy SM (1991) Hind limb movements of the American alligator (Alligator mississippiensis) and postural grades. J Zool 224:577–588. https://doi.org/10.1111/j.1469-7998.1991.tb03786.x
Gatesy SM, Biewener AA (1991) Bipedal locomotion: effects of speed, size and limb posture in birds and humans. J Zool 224:127–147. https://doi.org/10.1111/j.1469-7998.1991.tb04794.x
Gerkema MP, Davies WI, Foster RG, Menaker M, Hut RA (2013) The nocturnal bottleneck and the evolution of activity patterns in mammals. Proc R Soc Lond B Biol Sci 280:20130508. https://doi.org/10.1098/rspb.2013.0508
Germain D, Laurin M (2005) Microanatomy of the radius and lifestyle in amniotes (Vertebrata, Tetrapoda). Zool Scr 34:335–350. https://doi.org/10.1111/j.1463-6409.2005.00198.x
Gill PG, Purnell MA, Crumpton N, Brown KR, Gostling NJ, Stampanoni M, Rayfield EJ (2014) Dietary specializations and diversity in feeding ecology of the earliest stem mammals. Nature 512:303–305. https://doi.org/10.1038/nature13622
Girondot M, Laurin M (2003) Bone Profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. J Vertebr Paleontol 23:458–461
Gônet J, Laurin M, Girondot M (2022) BoneProfileR: the next step to quantify, model and statistically compare bone section compactness profiles. Palaeontol Electron 25:a12 https://doi.org/10.26879/1194
Gregory WK (1912) Notes on the principles of quadrupedal locomotion and on the mechanism of the limbs in hoofed animals. Ann N Y Acad Sci 22:267–294. https://doi.org/10.1111/j.1749-6632.1912.tb55164.x
Hastie T, Tibshirani R, Buja A (1994) Flexible discriminant analysis by optimal scoring. J Am Stat Assoc 89:1255–1270. https://doi.org/10.1080/01621459.1994.10476866
Hopson JA (2015) Fossils, trackways, and transitions in locomotion: a case study of Dimetrodon. In: Dial KP, Shubin N, Brainerd EL (eds) Great Transformations in Vertebrate Evolution. University of Chicago Press, Chicago, pp 125–141
Horovitz I, Ladevèze S, Argot C, Macrini TE, Martin T, Hooker JJ, Kurz C, Muizon C de, Sánchez-Villagra MR (2008) The anatomy of Herpetotherium cf. fugax Cope, 1873, a metatherian from the Oligocene of North America. Palaeontographica Abt A 284:109–141. https://doi.org/10.1127/pala/284/2008/109
Houssaye A, Botton-Divet L (2018) From land to water: evolutionary changes in long bone microanatomy of otters (Mammalia: Mustelidae). Biol J Linn Soc Lond 125:240–249. https://doi.org/10.1093/biolinnean/bly118
Houssaye A, Sander PM, Klein N (2016a) Adaptive patterns in aquatic amniote bone microanatomy—more complex than previously thought. Integr Comp Biol 56:1349–1369. https://doi.org/10.1093/icb/icw120
Houssaye A, Waskow K, Hayashi S, Cornette R, Lee AH, Hutchinson JR (2016b) Biomechanical evolution of solid bones in large animals: a microanatomical investigation. Biol J Linn Soc Lond 117:350–371. https://doi.org/10.1111/bij.12660
Houssaye A, Taverne M, Cornette R (2018) 3D quantitative comparative analysis of long bone diaphysis variations in microanatomy and cross‐sectional geometry. J Anat 232:836–849. https://doi.org/10.1111/joa.12783
Hu Y, Meng J, Wang Y, Li C (2005) Large Mesozoic mammals fed on young dinosaurs. Nature 433:149–152. https://doi.org/10.1038/nature03102
Hunt AP, Lucas SG (1998) Vertebrate tracks and the myth of the belly-dragging, tail-dragging tetrapods of the Late Paleozoic. N M Mus Nat Hist Bull 12:67–69
Hutchinson JR (2006) The evolution of locomotion in archosaurs. C R Palevol 5:519–530. https://doi.org/10.1016/j.crpv.2005.09.002
Hutchinson JR (2021) The evolutionary biomechanics of locomotor function in giant land animals. J Exp Biol 224:jeb217463. https://doi.org/10.1242/jeb.217463
Ibrahim N, Sereno PC, Dal Sasso C, Maganuco S, Fabbri M, Martill DM, Zouhri S, Myhrvold NP, Iurino DA (2014) Semiaquatic adaptations in a giant predatory dinosaur. Science 345:1613–1616. https://doi.org/10.1126/science.1258750
Isler K (2005) 3D-kinematics of vertical climbing in hominoids. Am J Phys Anthropol 126:6681. https://doi.org/10.1002/ajpa.10419
Jenkins FA (1971) Limb posture and locomotion in the Virginia opossum (Didelphis marsupialis) and in other non-cursorial mammals. J Zool 165:303–315. https://doi.org/10.1111/j.1469-7998.1971.tb02189.x
Jenkins FA (1973) The functional anatomy and evolution of the mammalian humero-ulnar articulation. Am J Anat 137:281–297. https://doi.org/10.1002/aja.1001370304
Jenkins FA, Parrington FR (1976) The postcranial skeletons of the Triassic mammals Eozostrodon, Megazostrodon and Erythrotherium. Philos Trans R Soc Lond B Biol Sci 273:387–431. https://doi.org/10.1098/rstb.1976.0022
Jenkins FA, Weijs WA (1979) The functional anatomy of the shoulder in the Virginia opossum (Didelphis virginiana). J Zool 188:379–410. https://doi.org/10.1111/j.1469-7998.1979.tb03423.x
Jones KE, Dickson BV, Angielczyk KD, Pierce SE (2021) Adaptive landscapes challenge the “lateral-to-sagittal” paradigm for mammalian vertebral evolution. Curr Biol 31:18831892. https://doi.org/10.1016/j.cub.2021.02.009
Kemp TS (2005) The Origin and Evolution of Mammals. Oxford University Press, Oxford. https://doi.org/10.1093/oso/9780198507604.001.0001
Kielan-Jaworowska Z, Hurum JH (2006) Limb posture in early mammals: sprawling or parasagittal. Acta Palaeontol Pol 51:393–406
Kielan-Jaworowska Z, Cifelli RL, Luo Z-X (2004) Mammals from the Age of Dinosaurs: Origins, Evolution, and Structure. Columbia University Press, New York
Kilbourne B, Hutchinson JR (2019) Morphological diversification of biomechanical traits: mustelid locomotor specializations and the macroevolution of long bone cross-sectional morphology. BMC Evol Biol 19:37. https://doi.org/10.1186/s12862-019-1349-8
Klein N, Sander PM, Krahl A, Scheyer TM, Houssaye A (2016) Diverse aquatic adaptations in Nothosaurus spp. (Sauropterygia)—inferences from humeral histology and microanatomy. PLoS One 11:e0158448. https://doi.org/10.1371/journal.pone.0158448
Kriloff A, Germain D, Canoville A, Vincent P, Sache M, Laurin M (2008) Evolution of bone microanatomy of the tetrapod tibia and its use in palaeobiological inference. J Evol Biol 21:807–826. https://doi.org/10.1111/j.1420-9101.2008.01512.x
Kurz C (2005) Ecomorphology of opossum-like marsupials from the Tertiary of Europe and a comparison with selected taxa. Kaupia 14:21–26
Laurin M, Canoville A, Germain D (2011) Bone microanatomy and lifestyle: a descriptive approach. C R Palevol 10:381–402. https://doi.org/10.1016/j.crpv.2011.02.003
Lebrun R (2018) MorphoDig, an open-source 3D freeware dedicated to biology. IPC5 Abstract Book:399
Lin Y-F, Konow N, Dumont ER (2019) How moles walk; it’s all thumbs. Biol Lett 15:20190503. https://doi.org/10.1098/rsbl.2019.0503
Main RP, Simons EL, Lee AH (2021) Interpreting mechanical function in extant and fossil long bones. In: de Buffrénil V, de Ricqlès AJ, Zylberberg L, Padian K, Laurin M, Quilhac A (eds) Vertebrate Skeletal Histology and Paleohistology. CRC Press, Boca Raton, pp 688–723
Meier PS, Bickelmann C, Scheyer TM, Koyabu D, Sánchez-Villagra MR (2013) Evolution of bone compactness in extant and extinct moles (Talpidae): exploring humeral microstructure in small fossorial mammals. BMC Evol Biol 13:110. https://doi.org/10.1186/1471-2148-13-55
Meng J (2014) Mesozoic mammals of China: implications for phylogeny and early evolution of mammals. Natl Sci Rev 1:521542. https://doi.org/10.1093/nsr/nwu070
Motani R, Schmitz L (2011) Phylogenetic versus functional signals in the evolution of form–function relationships in terrestrial vision. Evolution 65:2245–2257. https://doi.org/10.1111/j.1558-5646.2011.01271.x
Myhrvold NP, Baldridge E, Chan B, Sivam D, Freeman DL, Ernest SKM (2015) An amniote life-history database to perform comparative analyses with birds, mammals, and reptiles. Ecology 96:3109–3109. https://doi.org/10.1890/15-0846R.1
Nakajima Y, Hirayama R, Endo H (2014) Turtle humeral microanatomy and its relationship to lifestyle. Biol J Linn Soc Lond 112:719–734. https://doi.org/10.1111/bij.12336
Niemitz C (2010) The evolution of the upright posture and gait—a review and a new synthesis. Naturwissenschaften 97:241–263. https://doi.org/10.1007/s00114-009-0637-3
Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884. https://doi.org/10.1038/44766
Parrish JM (1987) The origin of crocodilian locomotion. Paleobiology 13:396–414. https://doi.org/10.1017/S0094837300009003
Pietersen DW, Jansen R, Swart J, Panaino W, Kotze A, Rankin P, Nebe B (2020) Temminck’s pangolin Smutsia temminckii (Smuts, 1832). In: Challender DWS, Nash HC, Waterman C (eds) Pangolins: Science, Society and Conservation. Elsevier, Amsterdam, pp 175–193. https://doi.org/10.1016/B978-0-12-815507-3.00011-3
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2021) nlme: linear and nonlinear mixed effects. R package version 3.1–153
Plasse M, Amson E, Bardin J, Grimal Q, Germain D (2019) Trabecular architecture in the humeral metaphyses of non-avian reptiles (Crocodylia, Squamata and Testudines): lifestyle, allometry and phylogeny. J Morphol 280:982–998. https://doi.org/10.1002/jmor.20996
Preuschoft H, Witte H, Christian A, Fischer M (1996) Size influences on primate locomotion and body shape, with special emphasis on the locomotion of ‘small mammals’. Folia Primatol 66:93112. https://doi.org/10.1159/000157188
Pridmore PA (1985) Terrestrial locomotion in monotremes (Mammalia: Monotremata). J Zool 205:53–73. https://doi.org/10.1111/j.1469-7998.1985.tb05613.x
Quemeneur S, de Buffrénil V, Laurin M (2013) Microanatomy of the amniote femur and inference of lifestyle in limbed vertebrates. Biol J Linn Soc Lond 109:644–655. https://doi.org/10.1111/bij.12066
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Regnault S, Fahn-Lai P, Norris RM, Pierce SE (2020) Shoulder muscle architecture in the echidna (Monotremata: Tachyglossus aculeatus) indicates conserved functional properties. J Mamm Evol 27:591–603. https://doi.org/10.1007/s10914-020-09498-6
Reilly SM, Elias JA (1998) Locomotion in Alligator mississippiensis: kinematic effects of speed and posture and their relevance to the sprawling-to-erect paradigm. J Exp Biol 201:2559–2574. https://doi.org/10.1242/jeb.201.18.2559
Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Rose KD (2006) The Beginning of the Age of Mammals. Johns Hopkins University Press, Baltimore
Rose JA, Sandefur M, Huskey S, Demler JL, Butcher MT (2013) Muscle architecture and out-force potential of the thoracic limb in the eastern mole (Scalopus aquaticus). J Morphol 274:1277–1287. https://doi.org/10.1002/jmor.20178
Russo GA, Kirk EC (2017) Another look at the foramen magnum in bipedal mammals. J Hum Evol 105:24–40. https://doi.org/10.1016/j.jhevol.2017.01.018
Scheidt A, Wölfer J, Nyakatura JA (2019) The evolution of femoral cross-sectional properties in sciuromorph rodents: influence of body mass and locomotor ecology. J Morphol 280:11561169. https://doi.org/10.1002/jmor.21007
Seilacher A (1970) Arbeitskonzept zur Konstruktions-Morphologie. Lethaia 3:393–396. https://doi.org/10.1111/j.1502-3931.1970.tb00830.x
Selva C (2017) Morphologie et fonction du système vestibulaire de l’oreille interne des mammifères souterrains. Dissertation, Muséum national d’Histoire naturelle, Paris
Sereno PC (2006) Shoulder girdle and forelimb in multituberculates: evolution of parasagittal forelimb posture in mammals. In: Carrano MT, Gaudin TJ, Blob RW, Wible JR (eds) Amniote Paleobiology: Perspectives on the Evolution of Mammals, Birds, and Reptiles. University of Chicago Press, Chicago, pp 315–366
Shannon CE (1948) A mathematical theory of communication. Bell Sys Tech J 27:379–423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
Shimer HW (1903) Adaptations to aquatic, arboreal, fossorial and cursorial habits in mammals. III. Fossorial adaptations. Am Nat 37:819–825. https://doi.org/10.1086/278368
Stadler T (2011) Mammalian phylogeny reveals recent diversification rate shifts. Proc Natl Acad Sci U S A 108:6187–6192. https://doi.org/10.1073/pnas.1016876108
Stein BR, Casinos A (1997) What is a cursorial mammal? J Zool 242:185–192. https://doi.org/10.1111/j.1469-7998.1997.tb02939.x
Stone M (1974) Cross-validatory choice and assessment of statistical predictions. J R Stat Soc Series B Stat Methodol 36:111133. https://doi.org/10.1111/j.2517-6161.1974.tb00994.x
Tommasini SM, Nasser P, Schaffler MB, Jepsen KJ (2005) Relationship between bone morphology and bone quality in male tibias: implications for stress fracture risk. J Bone Miner Res 20:1372–1380. https://doi.org/10.1359/JBMR.050326
Upham NS, Esselstyn JA, Jetz W (2019) Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biol 17:e3000494. https://doi.org/10.1371/journal.pbio.3000494
Vaughan TA, Ryan JM, Czaplewski NJ (2015) Mammalogy. Jones and Bartlett Learning, Burlington
Wagstaffe AY, O’Driscoll AM, Kunz CJ, Rayfield EJ, Janis CM (2022) Divergent locomotor evolution in “giant” kangaroos: evidence from foot bone bending resistances and microanatomy. J Morphol 283:313–332. https://doi.org/10.1002/jmor.21445
Wilson GP, Evans AR, Corfe IJ, Smits PD, Fortelius M, Jernvall J (2012) Adaptive radiation of multituberculate mammals before the extinction of dinosaurs. Nature 483:457–460. https://doi.org/10.1038/nature10880
Wright M (2018) Functional morphology of the hindlimb during the transition from sprawling to parasagittal gaits in synapsid evolution. Dissertation, Harvard University and University of Groningen
Acknowledgements
We warmly thank Alexandra Houssaye, Charlène Selva, Sandrine Ladevèze and Guillaume Billet for sharing with us the CT data of some of the studied specimens. We thank Joséphine Lesur, Géraldine Veron, Jacques Cuisin and Violaine Nicolas-Colin for granting us access to the MNHN collections. We are grateful to Renaud Lebrun and the MRI platform of the Université de Montpellier and to Marta Bellato and the AST-RX platform of the MNHN for their help in collecting CT data. We are indebted to Margot Michaud and Laura Bento Da Costa for their valuable advice and to Mathilde Aladini for her kind review of the manuscript. We are grateful to our two anonymous reviewers, whose comments helped to improve the quality of this study. We thank the Virtual Data initiative, run by the LabEx P2IO and supported by the Université Paris-Saclay, for providing computing resources on its cloud infrastructure.
Funding
This work was supported by the doctoral programme Interfaces pour le vivant (IPV), with the cooperation of Sorbonne Université, and by the ATM MNHN 2014 “formes possibles, formes réalisées”.
Author information
Authors and Affiliations
Contributions
JG collected the data, designed the study, performed the analyses, interpreted the results, wrote the manuscript. JB designed the analyses. MG designed the analyses. JRH interpreted the results. ML collected the data, designed the study, interpreted the results. All authors reviewed and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original online version of this article was revised: The body mass values reported in Table 1 and in Online Resource 1 were incorrectly displayed due to a switch in the separator between thousands and hundreds during the peer review process (from full stop to comma).
Supplementary information
Below is the link to the electronic supplementary material.
Online Resource 1
Microanatomical data for the studied taxa. (XLSX 26.0 KB)
Online Resource 2
Time-calibrated phylogenetic trees used in this study in Newick format. (ZIP 54.2 KB)
Online Resource 3
R script to repeat the results presented in this study and produce new postural inferences. (ZIP 941 Bytes)
Online Resource 4
R environment to repeat the results presented in this study and produce new postural inferences. (ZIP 232 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gônet, J., Bardin, J., Girondot, M. et al. Unravelling the postural diversity of mammals: Contribution of humeral cross-sections to palaeobiological inferences. J Mammal Evol 30, 321–337 (2023). https://doi.org/10.1007/s10914-023-09652-w
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10914-023-09652-w