Frog Origins: Inferences Based on Ancestral Reconstructions of Locomotor Performance and Anatomy
Total Page：16
File Type：pdf, Size：1020Kb
FOSSIL IMPRINT • vol. 72 • 2016 • no. 1-2 • pp. 108–116 (formerly ACTA MUSEI NATIONALIS PRAGAE, Series B – Historia Naturalis) FROG ORIGINS: INFERENCES BASED ON ANCESTRAL RECONSTRUCTIONS OF LOCOMOTOR PERFORMANCE AND ANATOMY ANTHONY HERREL1, 2, *, CÉCILE MOUREAUX1, MICHEL LAURIN3, GHEYLEN DAGHFOUS4, KRISTEN CRANDELL5, 6, KRYSTAL A. TOLLEY7, G. JOHN MEASEY8, BIEKE VANHOOYDONCK9, RENAUD BOISTEL10 1 UMR 7179 C.N.R.S/M.N.H.N., Département d’Ecologie et de Gestion de la Biodiversité, 57 rue Cuvier, Case postale 55, 75231, Paris Cedex 5, France. 2 Ghent University, Evolutionary Morphology of Vertebrates, K. L. Ledeganckstraat 35, B-9000 Gent, Belgium. 3 Département Histoire de la Terre, Muséum National d’Histoire Naturelle, UMR 7207 (CR2P), Sorbonne Universités, MNHN/CNRS/UPMC, France. 4 Groupe de Recherche sur le Système Nerveux Central, Département de Neurosciences, Université de Montréal, Montréal, Québec, Canada. 5 Field Research Station at Fort Missoula, Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA. 6 Department of Zoology, University of Cambridge, Cambridge, CB2 3EJ, UK. 7 South African National Biodiversity Institute, Kirstenbosch Research Centre, Rhodes Drive, Newlands, Private Bag X7, Claremont 7735, Cape Town, South Africa. 8 Centre for Invasion Biology, Department of Botany & Zoology, Stellenbosch University, Stellenbosch, South Africa. 9 Dept. Biology, University of Antwerp, Universiteitsplein 1, B-2610, Antwerpen, Belgium. 10 Université de Poitiers - UFR SFA, iPHEP UMR CNRS 7262, Bât B35 - TSA 51106, 6 rue Michel Brunet, 86073 POITIERS Cedex 9, France. * corresponding address: UMR 7179 C.N.R.S/M.N.H.N., Département d'Ecologie et de Gestion de la Biodiversité, 55 rue Buffon, 75005, Paris, France; e-mail: [email protected]. Herrel, A., Moureaux, C., Laurin, M., Daghfous, G., Crandell, K., Tolley, K. A., Measey, G. J., Vanhooydonck, B., Boistel, R. (2016): Frog origins: inferences based on ancestral reconstructions of locomotor performance and anatomy. – Fossil Imprint, 72(1-2): 108–116, Praha. ISSN 2533-4050 (print), ISSN 2533-4069 (on-line). Abstract: Frogs are the most species-rich and ecologically diverse group of amphibians and are characterized by a unique body plan including long legs, elongated ilia, and fused caudal vertebrae. Stem anurans such as Triadobatrachus or Czatkobatrachus have been suggested to have used jumping or hopping as part of their locomotor repertoire based on their anatomy. The earliest known true frog, Prosalirus bitis was suggested to have been a proficient jumper. However, data on jumping performance in frogs have never been used to attempt reconstruction of ancestral features at the base of the radiation. Here we provide data on jumping performance (forces and acceleration) in 20 species of extant frogs including representatives of most of the early radiating clades. We next use ancestral character value inferences to assess ancestral features. Our analyses suggest that frog ancestors were of small to medium size, had relatively short limbs, produced rather low jump forces, yet were capable of relatively high acceleration. Given the short limbs and low forces, the unique frog bauplan with a reduced vertebral column and a mobile ilio-sacral joint may not have been an adaptation for powerful jumping. Key words: Anura, locomotion, forces, anatomy, jumping Received: December 6, 2015 | Accepted: April 8, 2016 | Issued: August 15, 2016 Introduction including hoppers, jumpers, swimmers, burrowers, and arboreal walkers (Emerson 1978, Wells 2007). Moreover, Frogs are characterized by a unique bauplan that sets morphological convergence has been observed in species them apart from other amphibians. Unique features of with similar ecologies (Moen et al. 2013) suggesting that anurans include elongated hind limbs, an elongation of the iliac shaft, a transformation of the caudal skeleton into anatomy reflects the locomotor environment of these a rod-like urostyle, and the development of a mobile animals. Additionally, differences in jumping performance sacro-iliac joint (Emerson 1979, Jenkins and Shubin 1998). have been demonstrated in frogs with different ecologies The ecological context driving the evolution of this unique (Zug 1978). morphology has been debated and aquatic, riparian, and Stem anurans such as Triadobatrachus KUHN, 1962 or terrestrial origins have all been suggested (Gans and Parsons Czatkobatrachus EVANS et BORSUK-BIAŁYNICKA, 1998 have 1966, Lutz and Rome 1994). Modern frogs show a diversity been suggested to have used jumping or hopping as part of of locomotor modes despite their specialized anatomy, their locomotor repertoire based on their forelimb anatomy, 108 DOI 10.14446/FI.2016.108 which shares several features with anatomically modern Phylogenetic framework frogs (Sigurdsen et al. 2012). Based on the anatomy of the For comparative analysis, a timetree was compiled from frog-like deltoid attachment of the scapula, Sigurdsen and the literature. The topology and branch lengths reflect mostly co-authors suggested that these frogs used their forelimbs Bossuyt and Roelants (2009), although information from the to absorb landing forces. The lack of use of forelimbs du- fossil record was also used (e.g. Marjanović and Laurin ring landing observed in primitive frogs such as Ascaphus 2014). The absolute age of fossils was estimated using STEJNEGER, 1899 or Leiopelma FITZINGER, 1861 (Essner et a recent geological timescale (Gradstein et al. 2012). The al. 2010) was consequently interpreted as a derived feature branch immediately under a fossil is assumed to occupy at of this group. The Early Jurassic Prosalirus bitis SHUBIN least a whole geological age (most of which lasted between et JENKINS, 1995 has also been suggested to have been 2 and 12 Ma), which accounts for the uncertainty regarding a proficient jumper based on the anatomy of its pelvic girdle their true age, and (partly) for the fact that a clade is (Shubin and Jenkins 1995, Jenkins and Shubin 1998). These necessarily somewhat older than its oldest known fossil authors proposed an important role of the sacro-iliac record. Lissamphibian phylogenies more recent than Bossuyt articulation in allowing frogs to transmit forces from the and Roelants (2009) have been published, notably the tip appendicular to the axial system, thus helping create dating study by Pyron (2011), but these typically have fewer a powerful jump. A review of the pelvic and thigh anuran terminal taxa. Alternatively, we could have used only musculature in frogs (Přikryl et al. 2009) suggested that those with estimated node ages, which unfortunately would terrestrial jumping may have been the primitive mode of eliminate other recent studies from consideration (e.g., Frost locomotion from which other locomotor modes were et al. 2006, Pyron and Wiens 2013). However, these more subsequently derived. Moreover, they argued in favor of recent studies are generally congruent with Bossuyt and the importance played by the ilio-sacral articulation and Roelants (2009). We placed minimal time constraints into the associated musculature in the development of a jumping tree based on the age of the oldest fossil belonging to each locomotor mode. clade and molecular ages (Laurin et al. 2009). In the latter However, based on the fact that during development the case, we used the lower (most recent) boundary of the 95% muscles associated with the modified sacro-iliac joint mature confidence interval (CI) of the node ages as minimal after frogs have already assumed their typical locomotor constraint (Laurin et al. 2009). This calibration scheme, along mode, Fabrezi and co-authors (2014) argued that these with use of the Stratigraphic Tools (http://mesquiteproject.org/ modification are not needed for jumping per se. Additionally, packages/stratigraphicTools/ developed by Josse et al. in Reilly and Jorgensen (2011), based on a re-analysis of pelvic 2006) for Mesquite (https://mesquiteproject.wikispaces.com/ morphology across a broad sample of frogs, suggested that developed by Maddison and Maddison), can be used to the lateral bender, walker/hopper morphology of the pelvic stretch the branch lengths (within certain limits) over the girdle is basal for frogs and that long distance jumping whole tree in an objective (standardized) manner that allows must be considered as a derived feature which evolved branch lengths to reflect evolutionary time. To do this, the convergently in different frog lineages (see also Jorgensen minimal terminal and/or internal branch lengths can be and Reilly 2013, Reilly et al. 2015, 2016). Here we use increased using the Stratigraphic Tools. This can be useful measurements of jumping performance in extant frogs to when the phylogenetic independent contrasts are not reconstruct jumping performance at the base of the anuran standardized adequately over the initial tree. The terminals tree, specifically focusing on jumping forces and acceleration representing time constraints were pruned after standardi- as these are the traits most likely under selection (Emerson zation had been achieved, prior to character optimization. 1978). To do so we measured jump forces in 20 species of frogs with an emphasis on basal clades as these are especially Force plate recordings insightful in reconstructing ancestral states (see also Maximal jump forces for all species except Ascaphus Robovska-Havelkova et al. 2014). were measured using a piezo-electric force platform (Kistler Squirrel force plate; ± 0.1 N) as described previously