Finite element analysis; biting simulation; Felidae; Nimravidae; mandible biomechanics; Carnivora
Abstract :
[en] Cat-like carnivorans are a textbook example of convergent evolution with distinct morphological differences between taxa with short or elongated upper canines, the latest being often interpreted as an adaptation to bite at large angles and subdue large prey. This interpretation of the sabretooth condition is reinforced by a reduced taxonomic sampling in some studies, often focusing on highly derived taxa or using simplified morphological models. Moreover, most biomechanical analyses focus on biting scenarios at small gapes, ideal for modern carnivora but ill-suited to test for subduction of large prey by sabre-toothed taxa. In this contribution we present the largest 3D collection-based muscle-induced biting simulations on cat like carnivorans by running a total of 1,074 analyses on 17 different taxa at three different biting angles (30°, 60° and 90°) including both morphologies. While our results show a clear adaptation of extreme sabre-toothed taxa to bite at larger angles in terms of stress distribution, other performance variables display surprising similarities between all forms at the different angles tested, highlighting a continuous rather than bipolar spectrum of hunting methods in cat-like carnivorans and demonstrating a wide functional disparity and nuances of the sabretooth condition that cannot simply be characterized by specialized feeding biomechanics.
Fischer, Valentin ; Université de Liège - ULiège > Département de géologie > Evolution and diversity dynamics lab
Tseng, Z. Jack; UCB - University of California Berkeley [US] > Department of Integrative Biology > Functional Anatomy and Vertebrate Evolution Laboratory
Language :
English
Title :
Many-to-one function of cat-like mandibles highlights a continuum of sabre tooth adaptions
Publication date :
07 December 2022
Journal title :
Proceedings of the Royal Society. B, Biological Sciences
Turner A, Antón M, Salesa MJ, Morales J. 2011 Changing ideas about the evolution and functional morphology of machairodontine felids. Estudios Geologicos 67, 255-276. (doi:10.3989/egeol.40590.188)
Anton M. 2013 Sabertooth. Bloomington, IL: Indiana University Press.
Emerson SB, Radinsky L. 1980 Functional analysis of sabertooth cranial morphology. Paleobiology 6, 295-312. (doi:10.1017/S0094837300006813)
van Valkenburgh B, Jenkins I. 2002 Evolutionary patterns in the history of Permo-Triassic and Cenozoic synapsid predators. Paleontol. Soc. Pap. 8, 267-288. (doi:10.1017/s1089332600001121)
Gonyea WJ. 1976 Adaptive differences in the body proportions of large felids. Acta Anat (Basel) 96, 81-96. (doi:10.1159/000144663)
Akersten WA. 1985 Canine function in Smilodon (Mammalia, Felidae, Machairodontinae). Contrib. Sci. 356, 1-22. (doi:10.5962/p.226830)
Turner A, Antón M. 1997 The big cats and their fossil relatives: an illustrated guide to their evolution and natural history. New York, NY: Columbia University Press.
Antón M, Galobart À. 1999 Neck function and predatory behavior in the scimitar toothed cat Homotherium latidens (Owen). J. Vertebr. Paleontol. 19, 771-784. (doi:10.1080/02724634.1999.10011190)
Argot C. 2004 Functional-adaptive features and palaeobiologic implications of the postcranial skeleton of the late Miocene sabretooth borhyaenoid thylacosmilus atrox (Metatheria). Alcheringa 28, 229-266. (doi:10.1080/03115510408619283)
Andersson K, Norman D, Werdelin L. 2011 Sabretoothed carnivores and the killing of large prey. PLoS ONE 6, e24971. (doi:10.1371/journal.pone.0024971)
Slater GJ, van Valkenburgh B. 2008 Long in the tooth: evolution of sabertooth cat cranial shape. Paleobiology 34, 403-419. (doi:10.1666/07061.1)
Martin LD, Babiarz JP, Naples VL, Hearst J. 2000 Three ways to be a saber-toothed cat. Naturwissenschaften 87, 41-44. (doi:10.1007/s001140050007)
Matthew WD. 1910 The phylogeny of the felidae. Bull. Am. Mus. Nat. Hist. 28, 289-318. (doi:10.1007/bf01798035)
Figueirido B, MacLeod N, Krieger J, de Renzi M, Pérez-Claros JA, Palmqvist P. 2011 Constraint and adaptation in the evolution of carnivoran skull shape. Paleobiology 37, 490-518. (doi:10.1666/09062.1)
Figueirido B, Lautenschlager S, Pérez-Ramos A, van Valkenburgh B. 2018 Distinct predatory behaviors in scimitar-and dirk-toothed sabertooth cats. Curr. Biol. 28, 3260-3266.e3. (doi:10.1016/j.cub.2018.08.012)
Lautenschlager S, Figueirido B, Cashmore DD, Bendel EM, Stubbs TL. 2020 Morphological convergence obscures functional diversity in sabre-toothed carnivores: sabre-tooth functional morphology. Proc. R. Soc. B 287, 20201818. (doi:10.1098/rspb.2020.1818)
Chatar N, Fischer V, Siliceo G, Antón M, Morales J, Salesa MJ. 2021 Morphometric analysis of the mandible of primitive sabertoothed felids from the late Miocene of Spain Madrid. J. Mamm. Evol. 28, 753-771. (doi:10.1007/s10914-021-09541-0)
McHenry CR, Wroe S, Clausen PD, Moreno K, Cunningham E. 2007 Supermodeled sabercat, predatory behavior in Smilodon fatalis revealed by high-resolution 3D computer simulation. Proc. Natl Acad. Sci. USA 104, 16 010-16 015. (doi:10.1073/pnas.0706086104)
Piras P, Maiorino L, Teresi L, Meloro C, Lucci F, Kotsakis T, Raia P. 2013 Bite of the cats: Relationships between functional integration and mechanical performance as revealed by mandible geometry. Syst. Biol. 62, 878-900. (doi:10.1093/sysbio/syt053)
Janis CM, Figueirido B, DeSantis L, Lautenschlager S. 2020 An eye for a tooth: Thylacosmilus was not a marsupial 'saber-tooth predator'. PeerJ 2020, 1-36. (doi:10.7717/peerj.9346)
Bourke J, Wroe S, Moreno K, McHenry C, Clausen P. 2008 Effects of gape and tooth position on bite force and skull stress in the dingo (Canis lupus dingo) using a 3-dimensional finite element approach. PLoS ONE 3, e2200. (doi:10.1371/journal.pone.0002200)
Oldfield CC, Mchenry CR, Clausen PD, Chamoli U, Parr WCH, Stynder DD, Wroe S. 2012 Finite element analysis of ursid cranial mechanics and the prediction of feeding behaviour in the extinct giant Agriotherium africanum. J. Zool. 286, 171. (doi:10.1111/j.1469-7998.2011.00862.x)
Cox PG, Rinderknecht A, Blanco RE. 2015 Predicting bite force and cranial biomechanics in the largest fossil rodent using finite element analysis. J. Anat. 226, 215-223. (doi:10.1111/joa.12282)
Tseng ZJ, Grohé C, Flynn JJ. 2016 A unique feeding strategy of the extinct marine mammal kolponomos: convergence on sabretooths and sea otters. Proc. R. Soc. B 283, 20160044. (doi:10.1098/rspb.2016.0044)
Tseng ZJ, Su DF, Wang X, White SC, Ji X. 2017 Feeding capability in the extinct giant Siamogale melilutra and comparative mandibular biomechanics of living Lutrinae. Sci. Rep. 7, 1-10. (doi:10.1038/s41598-017-15391-9)
Lautenschlager S, Gill P, Luo ZX, Fagan MJ, Rayfield EJ. 2017 Morphological evolution of the mammalian jaw adductor complex. Biol. Rev. 92, 1910-1940. (doi:10.1111/brv.12314)
Püschel TA, Marcé-Nogué J, Gladman JT, Bobe RR, Sellers WI. 2018 Inferring locomotor behaviours in Miocene New World monkeys using finite element analysis, geometric morphometrics and machine-learning classification techniques applied to talar morphology. J. R Soc. Interface 15, 20180520. (doi:10.1098/rsif.2018.0520)
Rowe AJ, Rayfield EJ. 2022 The efficacy of computed tomography scanning versus surface scanning in 3D finite element analysis. PeerJ 10, e13760. (doi:10.7717/PEERJ.13760/SUPP-1)
Wroe S, McHenry C, Thomason J. 2005 Bite club: comparative bite force in big biting mammals and the prediction of predatory behaviour in fossil taxa. Proc. R. Soc. B 272, 619-625. (doi:10.1098/RSPB.2004.2986)
Dessem D, Druzinsky RE. 1992 Jaw-muscle activity in ferrets, Mustela putorius furo. J. Morphol. 213, 275-286. (doi:10.1002/jmor.1052130211)
Currey JD. 1987 The evolution of the mechanical properties of amniote bone. J. Biomech. 20, 1035-1044. (doi:10.1016/0021-9290(87)90021-2)
Currey JD, Brear K. 1990 Hardness, Young's modulus and yield stress in mammalian mineralized tissues. J. Mater. Sci. Mater. Med. 1, 14-20. (doi:10.1007/BF00705348)
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. (doi:10.1038/nature13622)
Erickson GM, Catanese J, Keaveny TM. 2002 Evolution of the biomechanical material properties of the femur. Anatomic. Rec. 268, 115-124. (doi:10.1002/ar.10145)
Grosse IR, Dumont ER, Coletta C, Tolleson A. 2007 Techniques for modeling muscle-induced forces in finite element models of skeletal structures. Anatomic. Rec. 290, 1069-1088. (doi:10.1002/ar.20568)
Dumont ER, Davis JL, Grosse IR, Burrows AM. 2011 Finite element analysis of performance in the skulls of marmosets and tamarins. J. Anat. 218, 151-162. (doi:10.1111/j.1469-7580.2010.01247.x)
R Core Team. 2021 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Wickham H. 2007 Reshaping Data with the reshape Package. J Stat Softw 21, 1-20. (doi:10.18637/jss.v021.i12)
Zeileis A, Grothendieck G, Ryan JA, Ulrich JM, Andrews F. 2022. Package 'zoo'. See https://cran.r-project.org/web/packages/zoo/index.html.
Revell LJ. 2012 phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223. (doi:10.1111/j.2041-210X.2011.00169.x)
Bapst DW. 2012 paleotree: an R package for paleontological and phylogenetic analyses of evolution. Methods Ecol. Evol. 3, 803-807. (doi:10.1111/j.2041-210X.2012.00223.x)
Bell MA, Lloyd GT. 2015 strap: an R package for plotting phylogenies against stratigraphy and assessing their stratigraphic congruence. Palaeontology 58, 379-389. (doi:10.1111/PALA.12142)
Yu G, Smith DK, Zhu H, Guan Y, Lam TTY. 2017 ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 8, 28-36. (doi:10.1111/2041-210X.12628)
Wickham H. et al.,. 2016. Package ggplot2: create elegant data visualisations using the grammar of graphics. See https://ggplot2.tidyverse.org/.
Kassambara A. 2020. ggpubr. See https://github.com/kassambara/ggpubr.
Paradis E, Schliep K. 2019 Ape 5.0: An environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526-528. (doi:10.1093/bioinformatics/bty633)
Barrett PZ. 2021 The largest hoplophonine and a complex new hypothesis of nimravid evolution. Sci. Rep. 11, 1-9. (doi:10.1038/s41598-021-00521-1)
Jiangzuo Q, Werdelin L, Sun Y. 2022 A dwarf sabertooth cat (Felidae: Machairodontinae) from Shanxi, China, and the phylogeny of the sabertooth tribe Machairodontini. Quat. Sci. Rev. 284, 107517. (doi:10.1016/j.quascirev.2022.107517)
Slater GJ, Friscia AR. 2019 Hierarchy in adaptive radiation: a case study using the Carnivora (Mammalia). Evolution (N Y) 73, 524-539. (doi:10.1111/evo.13689)
Tseng ZJ, Stynder D. 2011 Mosaic functionality in a transitional ecomorphology: skull biomechanics in stem Hyaeninae compared to modern South African carnivorans. Biol. J. Linnean Soc. 102, 540-559. (doi:10.1111/j.1095-8312.2010.01602.x)
Greaves WS. 1982 A mechanical limitation on the position of the jaw muscles of mammals: the one-third rule. J. Mammal. 63, 261-266. (doi:10.2307/1380635)
Anyonge W. 1996 Locomotor behaviour in Plio-Pleistocene sabre-tooth cats: a biomechanical analysis. J Zool 238, 395-413. (doi:10.1111/J.1469-7998.1996.TB05402.X)
Van Valkenburgh B. 1999 Major patterns in the history of carnivorous mammals. Annu. Rev. Earth Planet Sci. 27, 463-493. (doi:10.1146/annurev.earth.27.1.463)
Zhou Z, Winkler DE, Fortuny J, Kaiser TM, Marcé-Nogué J. 2019 Why ruminating ungulates chew sloppily: biomechanics discern a phylogenetic pattern. PLoS ONE 14, e0214510. (doi:10.1371/JOURNAL.PONE.0214510)
McCurry MR, Mahony M, Clausen PD, Quayle MR, Walmsley CW, Jessop TS, Wroe S, Richards H, McHenry CR. 2015 The relationship between cranial structure, biomechanical performance and ecological diversity in varanoid lizards. PLoS ONE 10, e0130625. (doi:10.1371/JOURNAL.PONE.0130625)
Ewer RF. 1998 The carnivores. Ithaca, NY: Cornell University Press.
Leyhausen P. 1979 Cat behaviour: the predatory and social behaviour of domestic and wild cats, 1st edn. New York, NY: Garland STPM Press.
Radloff FGT, Du Toit JT. 2004 Large predators and their prey in a southern African savanna: a predator's size determines its prey size range. J. Anim. Ecol. 73, 410-423. (doi:10.1111/j.0021-8790.2004.00817.x)
Slater GJ, Van Valkenburgh B. 2009 Allometry and performance: the evolution of skull form and function in felids. J. Evol. Biol. 22, 2278-2287. (doi:10.1111/j.1420-9101.2009.01845.x)
Berryman Scott W, Lowell Jepsen G. 1936 The mammalian fauna of the white river oligocene: part I. Insectivora and Carnivora. Trans. Amer. Phil. Soc. 28, 1-153. (doi:10.2307/1005507)
Bubenik GA, Bubenik AB. 1990 Horns, pronghorns, and antlers. New York, NY: Springer.
Ivakhnenko MF. 2008 Cranial morphology and evolution of Permian Dinomorpha (Eotherapsida) of eastern Europe. Paleontol. J. 42, 859-995. (doi:10.1134/S0031030108090013)
Ivakhnenko MF. 2005 Morphology of the Gorgonopidae (Eotherapsida) and Tetrapod communities in the Late Paleozoic. Paleontol. J. 39, S393-S511.
Rubidge BS, Sidor CA. 2001 Evolutionary patterns among permo-triassic therapsids. Annu. Rev. Ecol. Syst. 32, 449-480. (doi:10.1146/annurev.ecolsys.32.081501.114113)
Leinders JJM, Heintz E. 1980 Historical notes on the taxonomy and nomenclature of the recent Rhinocerotidae (Mammalia. Perissodactyla). Beaufortia 30, 155-160.
Capobianco A, Beckett HT, Steurbaut E, Gingerich PD, Carnevale G, Friedman M. 2020 Large-bodied sabre-toothed anchovies reveal unanticipated ecological diversity in early Palaeogene teleosts. R. Soc. Open Sci. 7, 192260. (doi:10.1098/rsos.192260)
Cisneros JC, Abdala F, Rubidge BS, Dentzien-Dias PC, de Oliveira Bueno A. 2011 Dental occlusion in a 260-million-year-old therapsid with saber canines from the permian of Brazil. Science (1979) 331, 1603-1605. (doi:10.1126/science.1200305)
Wainwright PC, Alfaro ME, Bolnick DI, Husley CD. 2005 Many-to-one mapping of form to function: a general principle in organismal design? Integr. Comp. Biol. 45, 256-262. (doi:10.1093/icb/45.2.256)
Chatar N, Fischer V, Tseng ZJ. 2022 Data from: Many-to-one function of cat-like mandibles highlights a continuum of sabre-tooth adaptations. Figshare. (doi:10.6084/m9.figshare.c.6308901)