Appendicular skeletons of five Asian skink species of the genera Brachymeles and Ophiomorus, including species with vestigial appendicular structures

in Amphibia-Reptilia
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Vestigial biological structures provide an important line of evidence for macroevolution. They abound in the appendicular skeletons of limbless and reduced-limbed members of the skink subfamily Scincinae, which includes a predominantly Asian clade and a predominantly African clade. Reduced appendicular skeletons in the predominantly African clade have received much recent attention, but for most species in the predominantly Asian clade the appendicular skeleton has yet to be described. Here we provide descriptions of the appendicular skeletons of the reduced-limbed skinks Brachymeles bonitae and Ophiomorus blandfordi, the externally limbless skink Ophiomorus punctatissimus, and, for comparison, the pentadactyl skinks Brachymeles gracilis and B. talinis. We used x-ray radiographs to examine the skeletons of these species and to note similarities and differences in the previously-described appendicular skeletal morphology of related species. We found that in B. bonitae the pectoral and pelvic girdles are unreduced, the proximal limb elements are reduced, and the distal limb elements are vestigial. In O. punctatissimus vestigial pectoral and pelvic girdles are present. In O. blanfordi the fifth metatarsal is vestigial. The phylogenetic distribution of morphological features related to appendicular reduction shows that multiple, parallel reduction events have taken place within each of these two genera. In addition, the anatomical distribution of element reduction and loss in these genera shows that the bones are reduced and lost in the same sequence in the predominantly Asian scincine clade as they are in other squamate clades. This suggests a common evolutionary mechanism for appendicular reduction and loss across the Squamata.

Appendicular skeletons of five Asian skink species of the genera Brachymeles and Ophiomorus, including species with vestigial appendicular structures

in Amphibia-Reptilia

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References

  • AndersonS.C.LevintonA.E. (1966): A review of the genus Ophiomorus (Sauria: Scincidae) with descriptions of three new forms. Proc. Calif. Acad. Sci. Ser. 4 33: 499-534.

    • Search Google Scholar
    • Export Citation
  • BrownR.M.McGuireJ.A.FernerJ.W.IcarangalN.Jr.KennedyR.S. (2000): Amphibians and reptiles of Luzon Island, II: preliminary report on the herpetofauna of Aurora Memorial National Park, Philippines. Hamadryad 25: 175-195.

    • Search Google Scholar
    • Export Citation
  • ConradE.C. (1982): True vestigial structures in whales and dolphins. Cr./Ev. 3 (4): 8-13.

  • CopeE.D. (1892): The osteology of the lizards. Proc. Am. Philos. Soc. 30: 185-221.

  • DarwinC. (1859): The Origin of Species by Means of Natural Selection or the Preservation of Favored Races in the Struggle for Life. John MurrayLondon.

    • Search Google Scholar
    • Export Citation
  • EssexR. (1927): Studies in reptilian degeneration. Proc. Zool. Soc. Lond. 4: 879-945.

  • FürbringerM. (1870): Die Knochen und Muskeln der Extremitäten bei den Schlangenähnlichen Sauriern. Wilhelm EngelmannLeipzig.

  • GansC. (1960): Studies on amphisbaenids (Amphisbaenia, Reptilia). 1. A taxonomic revision of the Trogonophinae, and a funcational interpretation of the amphisbaenid adapted pattern. Bull. Am. Mus. Nat. Hist. 119: 135-204.

    • Search Google Scholar
    • Export Citation
  • GoldbergE.E.IgićB. (2008): On phylogenetic tests of irreversible evolution. Evolution 62: 2727-2741.

  • HildebrandM.GoslowG.E.Jr. (2001): Analysis of Vertebrate Structure. John Wiley and SonsNew York.

  • KazemiS.M.QomiM.F.KamiH.G.AndersonS.C. (2011): A new species of Ophiomorus (Squamata: Scincidae) from Maranjab Desert Isfahan province, Iran, with a revised key to the genus. Amph. Rept. Conserv. 5 (1): 23-33.

    • Search Google Scholar
    • Export Citation
  • KearneyM. (2002): Appendicular skeleton in amphisbaenians (Reptilia: Squamata). Copeia 2002: 719-738.

  • LamarckJ.-B.P.A. (1809): Philosophie Zoologique. Duminil-LesueurParis.

  • LiniewskiR.StanelyS.AndradeJ.SenterP. (2015): Vestigial appendicular skeletons in the African and Malagasy skink species Feylinia grandisquamis, Melanoseps ater, Grandidierina lineata, and Voeltzkowia mira. Af. J. Herpetol. 65: 39-46.

    • Search Google Scholar
    • Export Citation
  • MirallesA.MiranaA.HipsleyC.A.MüllerJ.GlawF.VencesM. (2012): Variations on a bauplan: description of a new Malagasy “mermaid skink” with flipper-like forelimbs only (Scincidae, Sirenoscincus Sakata & Hikida, 2003). Zoosystema 34: 701-719.

    • Search Google Scholar
    • Export Citation
  • MirallesA.HipsleyC.A.ErensJ.GeharaM.RakotoarisonA.GlawF.MüllerJ.VencesM. (2015): Distinct patterns of desynchronized limb regression in Malagasy scincine lizards (Squamata, Scincidae). PLoS ONE 10 (6): e0126074.

    • Search Google Scholar
    • Export Citation
  • MochJ.G.SenterP. (2011): Vestigial structures in the appendicular skeletons of eight African skink species. Journal of Zoology 285: 274-280.

    • Search Google Scholar
    • Export Citation
  • OmuraH. (1980): Morphological study of pelvic bones of the minke whale from the Antarctic. Sci. Rep. Whales Res. Inst. 32: 25-37.

  • PostacchiniF.MassobrioM. (1983): Idiopathic coccygodynia. Analysis of fifty-one operative cases and a radiographic study of the normal coccyx. J. Bone Joint Surg. 65: 1116-1124.

    • Search Google Scholar
    • Export Citation
  • PyronR.A.BurbrinkF.T.WiensJ.J. (2013): A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 13: 93.

    • Search Google Scholar
    • Export Citation
  • RabanusK. (1911): Über das Skelett von Voeltzkowia mira Bttgr. Ein Beitrag zur Osteologie und Eidechsen. In: Reise in Ostafrika in den Jahren 1903-1905 mit Mitteln der Hermann und Elise geb. Heckmann Wentzel-Stiftung ausgefürt. Wissenschaftliche Ergebnisse. Band IV. Anatomie und Entwickelungsgeschichte. Heft 3 p.  279-330. VoeltzkowA. Ed. Schweizerbart’sche Verlagsbuchhandlung, Nägele und Dr. SproesserStuttgart.

    • Search Google Scholar
    • Export Citation
  • ReeceJ.B.UrryL.A.CainM.L.WassermanS.A.MinorskyP.V.JacksonR.B. (2011): Campbell Biology9th Edition. Benjamin CummingsBoston.

  • RenousS.GascJ.P. (1979): Etude des modalities de reduction des membres chez un Squamate serpentiforme: Scelotes, scincidé afro-malagasche (1). Ann. Sci. Nat. Zool. Paris 1: 99-132.

    • Search Google Scholar
    • Export Citation
  • SchmitzA.BrandleyM.C.MausfeldP.VencesM.GlawF.NussbaumR.A.ReederT.W. (2005): Opening the black box: phylogenetics and morphological evolution of the Malagasy fossorial lizards of the subfamily “Scincinae”. Mol. Phyl. Evol. 34: 118-133.

    • Search Google Scholar
    • Export Citation
  • SenterP.AmbriocioZ.AndradeJ.B.FoustK.K.GastonJ.E.LewisR.P.LiniewskiR.M.RaginB.A.RobinsonK.L.StanleyS.G. (2015): Vestigial biological structures: a classroom-applicable test of creationist hypotheses. Am. Biol. Teach. 77: 99-106.

    • Search Google Scholar
    • Export Citation
  • SenterP.MochJ.G. (2015): A critical survey of vestigial structures in the postcranial skeletons of extant mammals. PeerJ 3: e1439.

  • SewertzoffA.N. (1931): Studien über die Reduktion der Organe der Wirbeltiere. Zoologische Jahrbücher. Abt. Anat. Ontog. 53: 611-700.

    • Search Google Scholar
    • Export Citation
  • SilerC.D.BrownR.M. (2011): Evidence for repeated acquisition and loss of complex body-form characters in an insular clade of southeast Asian semi-fossorial skinks. Evolution 65: 2641-2663.

    • Search Google Scholar
    • Export Citation
  • SilerC.D.RicoE.L.DuyaM.R.BrownR.M. (2009): A new limb-reduced, loam-swimming skink (Squamata: Scincidae: Brachymeles) from central Luzon Island, Philippines. Herpetologica 65: 449-459.

    • Search Google Scholar
    • Export Citation
  • SilerC.D.DiesmosA.C.AlcalaA.C.BrownR.M. (2011): Phylogeny of Philippine slender skinks (Scincidae: Brachymeles) reveals underestimated species diversity, complex biogeographical relationships, and cryptic patterns of lineage diversification. Mol. Phyl. Evol. 59: 53-65.

    • Search Google Scholar
    • Export Citation
  • StephensonN.G. (1961): The comparative morphology of the head skeleton, girdles and hindlimbs in the Pygopodidae. J. Linn. Soc. Zool. 44: 627-644.

    • Search Google Scholar
    • Export Citation
  • StokelyP.S. (1947): Limblessness and correlated changes in the girdles of a comparative morphological series of lizards. Am. Nat. 38: 725-754.

    • Search Google Scholar
    • Export Citation
  • TagueR.G. (1997): Variability of a vestigial structure: first metacarpal in Colobus guereza and Ateles geoffroyi. Evolution 51: 595-605.

    • Search Google Scholar
    • Export Citation
  • WhitingA.S.BauerA.M.SitesJ.W.Jr. (2003): Phylogenetic relationships and limb loss in sub-Saharan African scincine lizards (Squamata: Scincidae). Mol. Phyl. Evol. 29: 582-598.

    • Search Google Scholar
    • Export Citation

Figures

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    Cladogram showing the relationships among genera of the skink clade Scincinae (Pyron et al., 2013; Miralles et al., 2015), including all species of Brachymeles and Ophiomorus, with states of limb reduction indicated. Bold font indicates species for which appendicular skeletons are described here, and an asterisk indicates species for which the appendicular skeleton has already been described. Black squares indicate externally limbless taxa; gray squares indicate taxa in which some but not all members are externally limbless. Black circles indicate digit loss; gray circles indicate taxa in which some but not all individuals exhibit digit loss; more than one symbol on a branch indicates a taxon in which multiple phenotypes are present; a five-pointed star on a branch with other symbols indicates a taxon in which some members are pentadactyl. All lineages unmarked by squares and circles are pentadactyl. Anatomical data for Ophiomorus and Brachymeles are from Greer and Wilson (2001) and Siler et al. (2011). Numbers in rectangles indicate digit formulae (e.g. “3/4” for species with three fingers and four toes). Phylogenetic relationships between genera are illustrated as per Pyron et al. (2013), with genus names of Madagascan skinks updated as per Miralles et al. (2015). Phylogenetic relationships between the species of Ophiomorus are as per Greer and Wilson (2001), and phylogenetic relationships between the species of Brachymeles are as per Siler et al. (2011).

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    Radiographs of Brachymeles gracilis (USNM 496798) (top) and B. talinis (USNM 228392) (bottom). The two boxes in the full-body radiographs indicate the position of the enlarged areas. The corners of the sternum are marked by small, white circles. c = carpal element, cl = clavicle, co = coracoid, h = humerus, i = interclavicle, il = ilium, is = ischium, m = metacarpal, mt = metatarsals, p = phalanges, pu = pubis, pub = puboischium, r = radius, s = scapula, st = sternum, sv = sacral vertebrae, t = tarsus, u = ulna.

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    Left and center columns: radiographs of Brachymeles bonitae: USNM 519333 (top), 519334 (middle), and 19345 (bottom). Right column: radiographs of Brachymeles bonitae (USNM 496945). The two boxes in the full-body radiographs indicate the position of the enlarged areas below. The corners of the sternum are marked by small, white circles. Abbreviations as in fig. 2.

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    Radiographs of Ophiomorus blanfordi (USNM 148660) (left column) and O. punctatissimus (USNM 31956) (right column). The two boxes in the full-body radiographs indicate the position of the enlarged areas below. The corners of the sternum are marked by small, white circles. Abbreviations as in fig. 2.

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