Direct-developing frogs: ontogeny of Oreobates barituensis (Anura: Terrarana) and the development of a novel trait

in Amphibia-Reptilia
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

Within Anura, direct development involves ontogenetic changes of the biphasic ancestral pattern. The recent partitioning of the genus Eleutherodactylus, along with the proposition of the unranked taxon Terrarana, has renewed an interest to the morphological and ecological diversity among direct-developing frogs. The morphological changes during embryonic development of Oreobates barituensis is similar to those of other Neotropical direct-developing species, including the reduction or absence of several larval and embryonic characters (e.g., external gills and adhesive glands), heterochronic changes (e.g., early developing limbs and late persistence of ciliated epidermal cells), and the appearance of new structures (e.g., egg tooth). The tail achieves an extraordinary peramorphic development (encloses the entire embryo), and the location of its expanded part is interpreted as a heterotopic change resulting in a novel trait. An enveloping tail with apparently non-heterotopic fins, combined with the absence of gills, has been only reported for a species of the related genus Craugastor, and these morphologies suggest an informative perspective for the study of evolution of direct development in terraranans.

Direct-developing frogs: ontogeny of Oreobates barituensis (Anura: Terrarana) and the development of a novel trait

in Amphibia-Reptilia

Sections

References

AdamsonL.HarrisonR.G.BayleyI. (1960): The development of the whistling frog, Eleutherodactylus martinicensis of Barbados. Proc. Zool. Soc. London 133: 453- 469.

AkmentinsM.VairaM. (2009): Amphibia, Anura, Strabomantidae, Oreobates barituensis: Distribution extension, new provincial record and geographic distribution map. Check List 5: 216- 217.

AkmentinsM.S. (2011): Vocal repertoire of two species of Oreobates Jiménez de la Espada, 1872 (Anura: Strabomantidae) of the Yungas Andean Forest, NW Argentina. J. Nat. Hist. 45: 1789- 1799.

AltigR.McDiarmidR.W. (1999): Body plan: development and morphology. In: Tadpoles: The Biology of Anuran Larvae p.  24- 51. McDiarmidR.W.AltigR. Eds Chicago and LondonUniversity of Chicago Press.

AnstisM.ParkerF.HawkesT.MorrisI.RichardsS.J. (2011): Direct development in some Australopapuan microhylid frogs of the genera Austrochaperina, Cophixalus and Oreophryne (Anura: Microhylidae) from northern Australia and Papua New Guinea. Zootaxa 3052: 1- 50.

ArthurW. (2011): Evolution: A Developmental Approach . John Wiley & Sons.

Bininda-EmondsO.JefferyJ.Sánchez-VillagraM.HankenJ.ColbertM.PieauC.SelwoodL.Ten CateC.RaynaudA.OsabuteyC.RichardsonM.K. (2007): Forelimb-hind limb developmental timing across tetrapods. BMC Evol. Biol. 7: 182.

BozzolaJ.J.RussellL.D. (1999): Electron Microscopy: Principles and Techniques for Biologists2nd Edition. MassachusettsJones and Bartlett Publishers.

CalleryE.M.ElinsonR.P. (2000): Opercular development and ontogenetic re-organization in a direct developing frog. Dev. Genes Evol. 210: 377- 381.

CalleryE.M.FangH.ElinsonR.P. (2001): Frogs without polliwogs: evolution of anuran direct development. BioEssays 23: 233- 241.

CrumpM.L. (1974): Reproductive strategies in a tropical anuran community. Misc. Publ. Mus. Nat. Hist. 61: 1- 68.

ElinsonR.P. (1990): Direct development in frogs: wiping the recapitulationist slate clean. Sem. Dev. Biol. 1: 263- 270.

ElinsonR.P. (2001): Direct development: an alternative way to make a frog. Genesis 29: 91- 95.

ElinsonR.P.Del PinoE.M.TownsendD.S.CuestaF.C.EichhornP. (1990): A practical guide to the developmental biology of terrestrial breeding frogs. Biol. Bull. 179: 163- 177.

FabreziM.QuinzioS.GoldbergJ. (2009): Giant tadpole and delayed metamorphosis of Pseudis platensis Gallardo, 1961 (Anura, Hylidae). J. Herpetol. 43: 228- 243.

FrostD.R. (2011): Amphibian Species of the World: an Online Reference. Version 5.5 (31 January 2011). Electronic Database accessible at http://research.amnh.org/vz/herpetology/amphibia/. American Museum of Natural History New York USA.

GitlinD. (1944): The development of Eleutherodactylus portoricensis. Copeia 1944: 91- 98.

GoldbergJ. (2009): Constancia y Variación en el Desarrollo de los Miembros en Anuros. Ph.D. Dissertation Universidad Nacional de Tucumán Argentina.

GosnerK.L. (1960): A simplified table for staging anurans embryos and larvae with notes on identification. Herpetologica 16: 183- 190.

HallB.K. (1999): Evolutionary Developmental Biology2nd Edition. BostonKluwer Academic Publishers.

HankenJ. (1999): Larvae in amphibian development and evolution. In: The Origin and Evolution of Larval Forms p.  61- 108. HallB.K.WakeM.H. Eds New YorkAcademic Press.

HankenJ. (2003): Direct development. In: Keywords and Concepts in Evolutionary Developmental Biology p.  97- 102. HallB.K.OlsonW.M. Eds CambridgeHarvard University Press.

HankenJ.JenningsD.H.OlssonL. (1997a): Mechanistic basis of life-history evolution in anuran amphibians: direct development. Amer. Zool. 37: 160- 171.

HankenJ.KlymkowskyM.W.AlleyK.E.JenningsD.H. (1997b): Jaw muscle development as evidence for embryonic repatterning in direct-developing frogs. Proc. R. Soc. Lond. B Biol. Sci. 264: 1349- 1354.

HedgesS.B.DuellmanW.E.HeinickeM.P. (2008): New World direct-developing frogs (Anura: Terrarana): Molecular phylogeny, classification, biogeography, and conservation. Zootaxa 1737: 1- 182.

HeinickeM.P.DuellmanW.E.TruebL.MeansD.B.MacCullochR.D.HedgesS.B. (2009): A new frog family (Anura: Terrarana) from South America and an expanded direct-developing clade revealed by molecular phylogeny. Zootaxa 2211: 1- 35.

JamesonD.L. (1950): The development of Eleutherodactylus latrans. Copeia 1950: 44- 46.

KerneyR.GrossJ.B.HankenJ. (2010): Early cranial patterning in the direct-developing frog Eleutherodactylus coqui revealed through gene expression. Evol. Dev. 12: 373- 382.

LynchJ.D. (1975): A review of the Andean Leptodactylid frog genus Phrynopus. Occas. Pap. Mus. Nat. Hist. 35: 1- 51.

LynnW.G. (1942): The embryology of Eleutherodactylus nubicola. Carnegie Inst. Wash. 190: 27- 62.

LynnW.G.LutzB. (1946): The development of Eleutherodactylus guentheri. Bol. Mus. Nac. Brasil 71: 1- 46.

MartojaR.Martoja-PiersonM. (1970): Técnicas de histología animal . BarcelonaToray-Masson S.A.

NinaL.H.Del PinoE.M.V. (1977): Estructura histológica del ovario del sapo Eleutherodactylus unistrigatus y observaciones sobre el desarrollo embrionario. Rev. de la Pontificia Univ Católica del Ecuador 5: 31- 41.

NobleG.K. (1925): An outline of the relation of ontogeny to phylogeny within the Amphibia. I. Amer. Mus. Novit. 165: 1- 45.

NokhbatolfoghahaiM. (2006): Embryonic surface ciliated cells in Eleutherodactylus urichi (Anura: Leptodactylidae). Iranian J. Sci. Tech. A 30: 133- 137.

NokhbatolfoghahaiM.DownieJ.R.ClellandA.K.RennisonK. (2005): The surface ciliation of anuran amphibian embryos and early larvae: patterns, timing differences and functions. J. Nat. Hist. 39: 887- 929.

NokhbatolfoghahaiM.DownieJ.R.OgilvyV. (2006): Surface ciliation of anuran amphibian larvae: persistence to late stages in some species but not others. J. Morphol. 267: 1248- 1256.

NokhbatolfoghahaiM.MitchellN.J.DownieJ.R. (2010): Surface ciliation and tail structure in direct-developing frog embryos: a comparison between Myobatrachus gouldii and Pristimantis (= Eleutherodactylus) urichi. Herpetol. J. 10: 59- 68.

PadialJ.M.De la RivaI. (2005): Rediscovery, redescription, and advertisement call of Eleutherodactylus heterodactylus (Miranda Ribeiro, 1937) (Anura: Leptodactylidae), and notes on other Eleutherodactylus. J. Herpetol. 93: 372- 379.

PadialJ.M.KöhlerJ.MuñozA.De la RivaI. (2008): Assessing the taxonomic status of tropical frogs through bioacoustics: geographical variation in the advertisement calls in the Eleutherodactylus discoidalis species group (Anura). Zool. J. Linnean Soc. 152: 353- 365.

PombalJ.P.Jr. (1999): Oviposição e desenvolvimento de Brachycephalus ephippium (Spix) (Anura, Brachycephalidae). Revta. Bras. Zool. 16: 967- 976.

PyronR.A.WiensJ.J. (2011): A large-scale phylogeny of Amphibia with over 2,800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol. Phyl. Evol. 61: 543- 583.

ReillyS.M.WileyE.O.MeinhardtD.J. (1997): An integrative approach to heterochrony: the distinction between interspecific and intraspecific phenomena. Biol. J. Linn. Soc. 60: 119- 143.

RichardsonM.CarlT.HankenJ.ElinsonR.CopeC.BagleyP. (1998): Limb development and evolution: a frog embryo with no apical ectodermal ridge (AER). J. Anat. 192: 379- 390.

SampsonL.V. (1904): A contribution to the embryology of Hyloides martinicensis. Am. J. Anat. 3: 473- 504.

SingamsettyS.ElinsonR.P. (2010): Novel regulation of yolk utilization by thyroid hormone in embryos of the direct developing frog Eleutherodactylus coqui. Evol. Dev. 12: 437- 448.

ThibaudeauG.AltigR. (1999): Endotrophic anurans: development and evolution. In: Tadpoles: The Biology of Anuran Larvae p.  170- 188. McDiarmidR.W.AltigR. Eds Chicago and LondonUniversity of Chicago Press.

TownsendD.S.StewartM.M. (1985): Direct development in Eleutherodactylus coqui (Anura: Leptodactylidae): A staging table. Copeia 1985: 423- 436.

ValettB.B.JamesonD.L. (1961): The embryology of Eleutherodactylus augusti latrans. Copeia 1961: 103- 109.

WakeM.H. (1989): Phylogenesis of direct development and viviparity in vertebrates. In: Complex Organismal Functions: Integration and Evolution in Vertebrates p.  235- 250. WakeD.B.RothG. Eds New York and ChichesterJohn Wiley.

WebsterM.ZelditchM.L. (2005): Evolutionary modifications of ontogeny: heterochrony and beyond. Paleobiology 31: 354- 372.

WellsK.D. (2007): The Ecology and Behavior of Amphibians . Chicago and LondonUniversity of Chicago Press.

Figures

  • View in gallery

    External development in pre-hatching stages of Oreobates barituensis. Jelly layers have been removed and contrast was increased with methylene blue. Stages of Townsend and Stewart (1985; TS) are indicated. (A) TS4, dorsal view. Note bulges of the gill arches and forelimbs. (B) TS5, dorsal, anterolateral, and rear views. Note the dermal fold at the base of the forelimb, and the lateral extensions of the tail. (C) TS6, dorsal view. The lateral extensions of the tail surround the embryo completely. Pictures within the square are details of the anterior and posterior parts once the tail extensions have been removed. (D) TS10-11, dorsal and posteroventral views. Note the highly vascularized tail extension with a small gap. (E) TS12-13, lateral view. Note the small gap in the tail extensions. (F) Same specimens as in D, with the tail extensions removed. Note the egg tooth and the dermal fold. (G) Same specimen as in E, with the tail extensions removed. Note the keratinized egg tooth. (H) TS13, ventral and lateral views, showing the tail regressing. (I) TS14-15, dorsal and lateral views, showing more advanced tail regression. DF: dermal fold; ET: egg tooth; FL: forelimb; G: gap in the enveloping tail; GA: gill arches; TE: tail extension; VT: vent tube. Scale bars = 1 mm.

  • View in gallery

    Post-hatching specimens of Oreobates barituensis. (A) Specimen with a vestige of the tail. (B) Specimen with the tail completely resorbed. Scale bars = 1 mm.

  • View in gallery

    Tail cross sections. (A) Scinax acuminatus pond tadpole. (B) Oreobates barituensis, tail distal portion with a detail of large blood vessels in the lateral extensions. The spinal cord/notochord axis is in line with the fins in (A) but perpendicular to the lateral extensions in (B); also note the large blood vessels in contact with the epidermis in Oreobates. BV: blood vessel; DF: dorsal fin; M: muscles; N: notochord; S: spinal cord; T: tail extension; VF: ventral fin. Scale bars = 1 mm (A) and 0.1 mm (B). This figure is published in colour in the online version.

  • View in gallery

    Scanning electron micrographs of specimens of Oreobates barituensis. (A) TS6, ciliated cells from yolk mass (left, as indicated by the asterisk) and detail of the ciliated hind limbs and vent tube (right). (B) TS12, ciliated cells from the nostril region (left, as indicated by the asterisk) and detail of the egg tooth (right).

  • View in gallery

    Plots comparing embryonic development of Eleutherodactylus coqui (dotted lines) and Oreobates barituensis (solid lines). (A) Rates of time development per stage of Townsend and Stewart (1985). Timing in E. coqui was taken from the original paper, and an average of the described developmental period (17-26 days) was used. Embryos were raised at comparable temperatures (20-25°C). Note that embryonic development in O. barituensis takes longer mainly because of an arrested rate at later stages. (B) Limbs and tail developmental events. The Y-axis represents shape stages in limb and tail development, described in two separate ordinal scales. Limb development is defined as the sequential differentiation of limb buds, elbows and knees, and toes, and finally toe elongation; note the similar onset and the isomorphic limb final shape achieved after a slower rate and a later offset in O. barituensis. Tail development is summarized as tail bud stage, full tail 70% the snout-vent length, and full enveloping tail; in O. barituensis, a peramorphic final shape results from an accelerated rate.

Index Card

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 15 15 5
Full Text Views 5 5 5
PDF Downloads 3 3 3
EPUB Downloads 0 0 0